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Variations in the relative abundance of the carbon isotopes in plants
Gewhimicr et Cosmochimica Acta, 1852, Vol. 2, pp. 243 to 254. PergamonPress Ltd., London
Var~a~ons in the relative abunda~e~ of the carbon isoto~s in plants* FRANS E. WICKMAN Riksmuseet,
Stockholm 50, Sweden
(Received 21 January
1952)
ABSTRACT The cl*/@ ratio of 105 plants mpmaenting 811the major system8tic groups has been dekmined. Except perhaps for gymnosperms there are in principle no systematic differences between the groups. Charscteristic differences occur, however, between plantsgrown in different biotopes, and these differences sre related to the varying intensity of the local carbon-dioxide cycle.
INTRODrrC!cIOW A. 0. NIER and his co-workers [l], [2] have shown that the isotopic composition of carbon in living matter and related materials is different from that in carbonates. So far the number of investigated plants is small, and in a compilation made by K. RANEAMA[3] in 1948 only seven examples of present day plants are presented. This material is too limited to be used as a starting-point for geochemical calculations of the circulation of carbon in nature, and in an effort to fill this gap in our knowledge the pr&ent investi~tion was started. THE MATERIAL The material consisted of plants from the herbarium of the Riksmuseum in Stockholm which had been preserved for periods of time varying between 1 and 115 years. However, this circumstance seems to have no influence on the results, judging from the fact that these do not vary s~tematically with the “herbarium age ” of the plant. This is not surprising if it is remembered that the preparation of a plant for a herbarium is merely s, drying process. The plants were burned with oxygen in a combustion furnace by A. PARVEL using the s&me technique as described by S. LANDEBUREN and A. PARVEL[ll]. Those plants con~i~ng calcium carbonate, e.g. Chara, were treated witn acid before being burned in order to avoid contamination from occluded calcium carbonate, The mass spectrometric measurements were performed by R. RYHAGE at the Department of Chemistry of the Karolinska Institut. The reproducibility of the measurements is within Ifr O-1 unit, in most cases within about &I*05 unit. The results are referred to the same standard sample used in the earlier papers of this series [4], [ci], f6]. Originally the intention was to have common representatives of all the major plant groups. Furthermore, the same species was to be represented by plants grown in very different surroundings, e.g. plants from the Northern and Southern limits of their distribution. The results obtained were so in~resti~~, however, that the material had to be completed using ecological instead of systematic viewpoints. They are presented in Table 1. *
Paper No. 5 in a series devoted to the application of isotope ratios to geological problems.
17 Oeochim. Vol. 2
243
Abbreviatkww;
m = marine;
NO.
1
2
-.
!&bk 1 d = desart plant; 1 = laoustrine;
-I_____.--
tr = tropical rain forest plant
Nome and toudity
C’yY
Ulva lactuca, Malmo, Sweden. . . . . . . . . . . . . . . , . 171va lactuca, f. &.&b, Venice, Italy . . . . . . . . . . . .
III III
Charoph~sae Ivetofta, Sk&me, Sweden . . . . . . . . . . . Uhuruf&i&, Sah, Argentine . . . . . . . . . . . . = . _ Uiboro fr&l&, Lake Ringsjiin, Sweden . . , . . . . _ . . . HI i%sra jzcbata, “Par%teiner See,” A~errn~~de, Germany. . . . Okra ~~~~a, ground, Sweden . . r , . . . _ . . . . . 7 3
Ohara crilaita,
8
Fuctba fur&us,
9
Bk.tw o~esimloeus,Varberg,
10 11 12
.
m
. . .
1 1 1 ni
_
f. vatiiEi8,
Sitka, Ah&s, , . . . . . . . . . . Sweden . . . . . . . . . . . . . . between St. Paul and Amsterdam, Atlantic
Macracy&s pyrifera, Ooean * . a . . . . . . . . . . . . . . . . . . . . . . . &wgamm gMu!&a.efoEium, Sidney, New South Wale8 . . . . Sargawum nakz?as, Sargasso Sea, Atlantic Ocean . . . . . . . . Rhodophweae i&spue, Eristineberg, Bohm&&n, Sweden . f . . . 1 . Cho9&-as m&p8, Digby Neck, Nova, Scotia . . . . . . _ . . .
13 14
~butrus
17 18 19 20 21
&brchau& Marchantia Xarcha&.a, Plagioahika Pkgiochila
22 23 24 25 26
Hy~~~rn 8~~~~6, Ryd, V&8tergothmd, Sweden . . dioEdorpn e&y&, Rydboholm, Uppl~nd, Sweden. . . . . Sp~~rn f~~~~~, Fiord0 Martine8, Bahia Pliischow, upturn ~rg~oh~~~, Ydre, Sweden . . . . . . _ . . Sp&r~m, Taemania I . . . . . . , . . . . . . . .
27 23 29 30
Ptem’doph~tu 1. Lycopodinme Lycopodaum selego, Caldas, Minas Geraes, Braeil . . Lycopo&um s&go, Restock, Dalsland, Sweden . . Sekxginella sekaginoides, Forssa, Hiilsingland, Sweden Se&&elk selagi,noides, Canada . . . I , . .
31 32 33
Ugathea aMra&s, Atherton Tableland, N. Queer&and . ~ _ . . Bryopteris the~yp~, Danderyd, Sweden . . . . . . . . . . . Bryvpterie t~~~~, SE side of Hibmanjaro, Eitet Africa _ . .
borteroana, Puyehue, Osorno, Chile , , , polymorpha, Halltorp, SmAlland, Sweden Tasmania . . , . . . . . . . . . . . aepEenioides, Hjnleerud, Sweden . . . . cava. Caldas, Minas Gerabs, Bra4 . . .
89.37 90.30 90-03 9043 9043
m m Ill
m nl
III III
. . . . _ . . . . . . . . . . . , ,
. . . . . . . . . . . .
2. Nusci
244
. . . . . . Chile . . .
. f
. .
. _ . .
. . . ‘. . . . . . . . . . . . _ . . . . .
. . . . . . .
90.76 90% 00.55 90-96 91.37
Nb79 9143 90.72 90.84
90.96 90.99
90*5x
Variations in the relative abnndence of the arbon
isotopes in planta
Table 1. (Continued) Name
No.
and
T
locality
O’/Q’
-7
Phanewganuw A. Bymnospermm 1. cyeudinut?
34
Uya~
me&u, Darwin, N. Terr., Australia
. . . . . . . . . . . .
90.48
36
2. (3inkgoim.e aiinkgo biloba,Kiangsi,mina . . . . . . . . . . . . . . . . .
90.70
36 37 38 39 40 41 42
A~azccaria angu&folicl, Rio Grande do Sul, Brazil . . . . . . Araucati biramdata, New Caledonia . . . . , . . . . . . . P&a abkx, T&by, Uppland, Sweden . . . . . . . . . . . . Pieeta e8perat4, Radja and Yellow River gorges, Eastern Tibet Pinru, silve8tri8, NW of Troizkosavsk, Transbaikalia . . . . . Podocarpue gradion, Kirstenbosch, Cape Province, S. Africa Podocar~s totara, Waitakera Hills, North Island, New Zealand
3. Cmiftxw . .
. . . . . .
90.62 90.49 90.67 90.80 90.64 90.62 90.63
. . . . . .
Be Angiospermae a) Dictyledoneae
43 44 46
1. Polycarpicae Brosenia 8ehrebev-i. Fish Lake, Chisago Co., Minn., U.S.A. . . Trigynaea eeua&ren8& between Tena and Napo, Prov. Napo stasa, Ecuador . . . . . . . . . . . . . . . . . . . . . Vdrola paponie, Tingo Maria, Prov. Hu&nuco. Peru . . . . .
1
89.26
. . . .
tr tr
91.27 90.88
Ck&gonurn acadhopterum, var. eetosa, between Annaju and Gnaurs, Askhabad. . . . . . . . . . . . . . . . . . . . . . . . . .
d
89.63
d d d
89.66 89.66 89.69 90.87 90.81
. . Pa-
2. Polygon&8
46
3. ccntroqi?lwl&?
47 48 49 60 61
Arthrophytum wborerrcenu, Repetek, Merv, Ealoxylon aphylLum, Central Asia . . . &duoh richteri, Repetek, Transcaspia . . Nd.lati media, LjusterS, Sweden . . . Stellaria media, Misserghin, Algeria . . .
62 63
kda cym.osa, Iquitos, Dep. Loreto, Peru . . . . . . . . . . . Tamariz androeetii, Amu-Darya, Turkestan . . . . . . . . . .
tr d
91.09 90.71
64 66
ChTy8odbkZmy8 weberbaueri, Tingo Maria, Dep. Huanuco, Peru . . . Dipterocarpus akztus, near Calcutta, Bengalia, India . . . . . . .
tr
91.12 90.72
66 67 68
Aetragalu8 pauci jugtu, Uch-A j ji, Transcaspia . . . . . . . . . . . Entadopeis polyphytla. Iquitos, Dep. Loreto, Peru . . . . . . . . Sckrolobium, !i”ingo Maria,Dep. Hu$nuco, Peru . . . . . . . . .
d tr tr
90.66 91.12 90.71
1
90.30
Transcaspia
. . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . _ . . .
. . . . . . . . . . . .
4. Parietake
6.
‘7.
Ro8lde8
hdQ8tGmod48
Poddemum ceratophyllum, on rocks, St. Regis River, Hogansburg, FranklinCo.,N.Y.. . . . . . . . . . . . . . . . . . . . .
245
.L
60 61 62 63 64 66 66 67
8. Nyrtales sne%dora, Warrumbungle Rsngee, New South Wales I Emzlyptw pol~lonthemos,Canbma, Auetrdia . , . . . . . . . Eugmia buxifolia, Key West, Florida, U.S.A. . . . . . . . . . . Eugenia mdcrophylla,Lantao I&nd, Kwangtung, China . . , . &tr~adderoe ongdijolia, Bosch Kloof, South Africa . . . . , . . 4%kOeidslroe poiyneorpha, subep. iwna, Huehue, Island of Hawaii. ~~hy~~ mm%eiWum, Atvidaberg, Sweden . . . . . . . . . Hippsti ~~T~~~ Friggesund at River Svhga,H~~~gl~nd, Sweden Mypius
1 1
9. Fagales 68 69 70 71 72 73
Bet&, %&&ad, Sweden . . . . . , . . . . . . . . . . . I s B&&Z emmi, Petropaviovak, Kamtchatka, twig. . . . . . . ~ . B&&b emnuni, Petropavlovsk, Kamtehatka, leaf . . . . . . . . .
9tm’J 9144 90.90 90.56 90.70 9WR7
Punta Arenaa, Patagonia. . . . . . . I . . Djebel’Ballota, Tunis . . . . . . . . . . . . . . . QWTW robw, Riainge, tistergfitland, Sweden . . . . . . . . . I
Nothofague
t&emu
bstuloidae
ikz,
10.
micalea
74 76
F&M paraw&, Quietocecba, Iquitos, Dep. Loreto, Peru . . ~ . . 0lmedi.a aepwa, Tingo Maria, Dep. Hu$nueo, Peru . . . . ~ . . .
76 77
Pr&a
78
Pierolemmo
79 80
Cork wdosa, Tingo Maria, Dep. Wu&nn\leo, Peru . . . . . . . . Jacaw~.& copaia, Tingo Maria, Dep. Hu4nuc0, Peru , . . . . . .
81
Sommera sabicsoides, Hacienda Sale&d, fquitoa, Dep. Loreto, Peru
82
Aobd& acne,
tr tr
11. Pro&.?&% ~y~~~~
.Proi+s ~~~,
&x&e B&en, Eritrea . . . . . . . m . . . . ~
Karoo Poort, South Africa
. . . . . . . . . .
12. Terebintak 8~rtccci,
Iquitos, Rep.
hF&O,
Peru
. . . * . . . . .
tr
914%
13. Tubiflorw t,r t#r
14. Rrbiales
15. CampcsnautcPtae Lake L&j& Vrena, S~de~an~nd,
Sweden .
tr
91.27
I
90.74
bf Monocotyledoneae 1. HeMiae Butamue umbeU.atuu,Lake Kolbotten, Naeka, Sweden. . . . . ~ I 83 Flottiund, Uppsala, Sweden . . . . . . . . . 84 i?Boda m&is, . . I . sz5 VaUisneria am&cam, Farleip Point, Cayuga Lake, N. Y.
9OM 90.2’; R9.9 1
2. P0tamo@mbale8
Naj@a mc;cr&wl, Laduviken, Stockholm, Sweden. h&mwpton dclwns, Irrigation e&m&l,Domoecua, by& : : : : Pdwwgs&m wfa~~, Eneta damm, G-amla Up@, Sweden . . l”o~ pectisauttae,the Sea S of Ski@nge, 8kkt5, Sweden Pofsmopb poEygosw, Ciddaa, Mkiss Gtyriss, Brazil . . . . . 91 Zoebpa III4pjwQ.Buccaritta, Fiume . . . . . . . . . . . . . 9% ZfMera 9ntwinu, v. a~~fo~, Styrraii,Bohuaiiin, Sweden. . .
a4 87 88 89 90
246
: 1 I .
. 1
I
90.18 90.85
1
90+51 89.47 9Im 89-W
1
. . .
111
. . j
m
I : ’
1 m
/
1 89.32
Variations
in the relative abundance of the carbon isotopes in plants Table I. ~co?i,f~~~~~
I
iName and Eocolity
No. -_
-1
.-
3. Pritipee
I
tr
90-89
tr
91.39
. . . . . . . . . Wolff&z urrhiza, St&~&nt water at Dunaharaszt~, Danube, Rounl%nia
1 1
91.04 90.88
6. Parve Typhu anguatifotia, Lake Normjon, Bladitker, Uppland,
. .
1
9036
Laaeiaeis ligulaia, San Juan, Iquitos, Dep. Loreto, Peru . . . . . . Paspalum distichwm, Stanford Univ. Lake, Santa Clara Co., Cal, U.S.A. 100 Paepalum diatichwm, Fiscbhoek, Cape Peninsula, South Africa . . .
tr 1 1
93
Degnboncu.s prunifer,
Jquitos, Dep. Loreto,
Peru
. . . . . . . . .
.
94
95 96
97
4. Synanthue Carludovica palm&a, Hacienda Clementina on Rio Pita, Prov. LOS Rioa, Peru . . . . . . . . . . . . . , . . . . . . . . . . .
5. Spathiflorae Lemna minor, M&ls&ker, S~dermanland, Sweden
Sweden
98 99
8. Gypera& 101 Carex 102 103
Andes NW of San Juan, North Argentine . . . . Carex Leporina, Kiisna, Bohusliin, Sweden . . . . -. . . . . , . . Dipbsia kar~t~~ol~a, Tingo Maria, Dep. HuBnuco, Peru . . . . . .
tr
9059 90.79 91.24
tr
90.64
~RCUTW,
9. gr~~~8 104
acne edwtrdi. Hacienda C~e~ent~na on Rio Pita, Prov. Los Rioe, Peru . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10. Liliijl4m.M 105
Eichkornia erassipes, in the swamp *‘La Siganea,” Catelina, Pinar de1 Rio, Cuba . . . . . . . . . , . . . . . . . . . . . . . .
90.91
I
L.
i
PRELIMINARY DISCUSSION OF THE RESULTS
The results of ‘NUB and his co-workers indicebtedthat there might be large variations in the CY/CY ratio of plants, and Table 1 is & confirmation of their results. There are several examples of the same species from two different localities, but they do not show any definite relatio~hip between isotope ratio and latitude, as can be seen from Table 2. It might therefore be conelnded that the ambient temperature is of no primary importance. On the ether hand if the material is divided into several groups such as marine plants, limnic plants, terrestrial plants from tropical rain-forests, desert plants, and other terrestrial plants, the distribution shown in Fig. 1 will be obtained. From this figure it is quite evident that some of the groups are quite homogeneous, especially marine plants, tropical rain-forest trees, rendthe group “other terrestrial plants.” If this lest-mentioned group is divided into three main subgroups : angiosperms, gymnosperm8 and cryptogames, it is interesting to note that two of the three groups show almost identical distribution, but that the third one, i.e. gymnosperms, sys~m~ti~lly gives somewhat lower ratios. Whether this trend is real or is due only to an u~avourable selection of plants, is impossible to determine with 247
F.E. WICICMAH
LOCddy
Plant d?pe&?
Italy ........... Sweden .........
45” lG 5P .K
Nova Scotia . . . . . . . Sweden. . . . = . . . . .
4P N 6O"N 5PN 59 "K 20" Y 60"h' 50"fX 60"N
Bring&o&a, Sweden Mariefred, Sweden. Brazil 1 _ . . . . Sweden . . . . . Canada . . . . . . Sweden . . . . . East Africa. SWedSXl
.
. . . ~ 1 .
. . . _ _ .
. . . . . .
. I . . . .
. . . . . . . .
.
s
.
.
.
.
.
Algeria. _ _ . . . . . . . Swe&x3 * : . . . . . . . California ........ South Africa .......
:
:
5O s 60'N 35"E 60°N
'
35ON 35"s
any degree of certainty from the limited material so far studied, but it may quite well be that this trend really exists. The desert plants show two wee-defied groups of values. It is in~res~ing to note that the 89*6-group grew in real deserts, the 9006-group in one case close to a river, in the other at a railway station. The limnic plants form a very heterogeneous group. It consists of (a) @ants which are rooted at the bottom and raised into the air at the top, and fb) submerged hydrophytes which live in deeper water. The emergent hydrophytes usually contain less chloiophyll in the submerged portion than in the portion above water. We may regard the floating hy~o~h~s, which are r&ted to the bottom but float their foliage upon the surface of the water, as a transition stage between these two groups. In all three cases the water in which the plants live may be stagnant or not. In Table 3 the limnic plants have been ciaasified according to the a~ve-mentioned properties, and an inspection of this table shows that isotope ratios around 91 are found far all plants living in stagnant water. On the other hand most submerged plants living in non-stagnant water give vaiues under 9@6, and the emergent hydrophytes elm form an i~omogen~~ group (Fig, 2). Before discus&g these results it might be profitable to recapitulate a few facts about the local carbon dioxide cycle. TEE
CYCLE OF CARBON
WITH SPECIAL REFEBEXWE TO
PLANTS
For over a hundred years the cycle of carbon in nature haa been studied by practically all hinds of soientists, and it is now known that it consists of a series of smaller cycles for~g a rather intrkate system. 248
Variations in the relative abundance of the esrbon isotopes in plsnts Table 3 Name
1
2
f e B 8 5 f 6 e/s f 6 6 8
ns ns ns n6 n8 6 n5 sjns (8) nu 6 n8 ns ni3 6 ns 6 sjns ns 8
C’fp
_-. 43 83 4 5 6
105 84 67 95 82 66 86 99, 100 59 87 88 90 97 85 96
Brasenia schreberi ............ Butomus umbelbtus ........... Chara foetida ............... Chara fragilis .............. Chara $~bata ............... Eichhoka crassipes ........... Eloeda eanudensis ............ EippwG ~~aT~8 ............ &mm rn~~. ............. ~bel~a ................ ~~ophyll,um ve~~~~t~v~ ........ Najas marina. ............. Paspalum distiehum ........... Podostemum ceratophyllum ........ Potamogeton densus ........... Potamogeton natans ........... Potamogeton pol ygonus .......... Typha anguatifolia ........... Vallisneria americana .......... Wolffia arrhiza .............
(:I 6 f 8 e 8 f
89.25 90.86 90.30 90.03 90.03 90-91 90.2i 91-01 91-04 90-74 91.16 90.18 89.51, 89.53 90.30 90.85 90.51 91.05 90.86 89.91 90.88
1. e = emergent hydrophyte; f = floating hydrophyte; 8 = submersed hydrophyte. 2. 6 = living in stagnant water; ns = living in non-stagnant water. i
In the present: paper we are concerned only with plants and therefore all other aspects of the carbon cycle will be neglected. The terrestrial plants obtain their carbon dioxide from the air, the mean content, of which is about O-03 ~01% . Depending on local factors which hardly can be account ed for in all specific cases, large variations around this mean value have been observed. However, some regularities have been noticed which are of special interest in connection with the carbon-dioxide fixation by plants. VON FODOR in 1881 was the first to observe that there is a daily periodicity in the CO, content of air, the maximum occuring during the night and the minimum during day time. This pronounced effect shows that the mixing between the main atmospheric air and the air layers close to the ground is not i~tan~neous, i.e. that diffusion is a slow process. It is also well-known that the air layer in immediate contact with the soil is enriched in carbon dioxide. The reason for this is that the soil produces carbon dioxide partly by the respiration of the microorganisms in the soil itself and partly by the respiration of the plant roots. There seems to be general agreement among botanists that the assimilation and production of carbon dioxide in a forest or other biotope are normally in equilibrium with each other. The soil, the atmosphere and the plants constitute the participants of the local cycle of carbon which is characteristic of plant life. Of course, their relative importance varies according to local conditions. Of great interest in this cycle is its completeness, i.e. to what degree the soil carbon-dioxide is directly assimilated by the plants. It is obvious from what has been said above that this process is 249
more complete if the plants are low-grown and live in an area under lee, especially if the carbon-dioxide produotion of the soil is high. On the other hand if a plant lives isolated from other plants in a windy place on an oceanic island, or in sand without muoh soil, it will generally obtain practically all of its carbon-dioxide supply from the main atmospheric air. These two examples are extreme c&8es,end 8s a rule conditions are somewhere in-between. Probabljt the first case will be most closely realized in a tropical rainforest, and the second in a desert. For hydrophytes there are several cases which should be discussed separately. First of all there are the emergent hydrophytes which are rooted to the bottom of the lake or the sea, but assimilate mainly atmospheric carbon dioxide. In most respeots they are equivalent to terrestrial plants, except for one thing which will be discussed below. The second group consists of submersed plants and the third of floatiug hydrophytes. This third group, to which e.g. water-lilies belong, are probably ~1-1~ related to the second one, because they do not extend to any height above the water surfaoe, and it might confidently be assumed that the carbon dioxide content of a very thin byer close to the water surface will be determined by the oarbon dioxide of the water. The submersed plants obtain their supply of carbon dioxide from the water. As is well-known, water contains carbonate ions, bicarbonate ions and dissolved carbon dioxide gas. There hresbeen much discussion among botanists and physiologiets ae to whether the plants a&milate the gas exclusively, or whether they are able to uee tbe ions directly. For the present discussion this point ia not important, since we &re primarily interested in isotope ratios which will not vary on account of the exobange of carbon stems between the different molecules and/ions. The total content of carbon dioxide in sea water varies greatly, but a normal value ia about 0.6 ~01%) i.e. the concentration is about ten times &s high as in the etmosphere. In lakes and rivers the content is also greatly variable, but for pure water in oor@ot with air the content is about 0.03 vol%, which means that it is the mrne as in air. ‘If the partial pressure of carbon dioxide is higher the amount of gas in the water will be lerger, and the same is true if the water is buffered by the .preaence of carbonates. In the open sea the carbon dioxide, produced at the bottom by microorganisms and by the reepiration of plants and eninarrle,will not have the same possibility to influence dire&y the clssimilation of submersed and emergent plants partly on socount of the &u&&ion of water by currents and partly on the high content of carbon dioxide present in se& water. However in a small stagnant part of the sea or lake or in a small pond, the conditions for a submersed plant will be almost the Borne as for a terrestrial plant. There will be an exchange of carbon dioxide with the atmosphere, and perhap also by convection currents with the main part, of the water beain. Finally there will be a supply of carbon dioxide with the groundwater, and this source might be of speaial importance in the ~888 of small springwater lakes without influx. If limestone is present in the area where the plant is living some of the rtssimilated carbon dioxide might derive from diaintegmted or dissolved rock material. The importance of this factor will of course vary oonsidembly according to local oircumtinces. 250
Variationsin the relativeabundanceof the carbonisot.opes in plants DISCUSSION OF THE RESULTS WITH SPECUL REFERENCE TO THE CYCLE OF CARBON DIOXIDE According to a statement of WEIGL [9] (cited after [S]) the assimilation rate of @‘O, is about 17 % less than that of C?O,. Probably this would correspond to a value somewhat around 5 % in the case of CY30,, which is a very serious discrepancy if one remembers that the pzaximum enrichment found in the present investigation is about 2 % . WEIQLB experiments are, however, very difficult to perform, on account of the simultaneous respiration and reassimilation of carbon dioxide by the plant, and his results cannot therefore be regarded as conclusive. The results of the present and earlier measurements on plants confirm, however, the reality of such a difference in the assimilation rates of the carbon dioxide molecules, but the observed effects are small. It might be asked whether the difference in the assimilation rates is alone responsible for the complete enrichment (one-step process), or whether the cycle of carbon dioxide, too, is essential in order to obtain the observed enrichments (cyclic process). Assuming the first alternative to be correct there are two possible theories. First, it might be thought that the difference in assimilation rates varies from species to species, or perhaps from plant to plant. Large differences should then be expected between e.g. ordinary plants, and xerophytes, and especially hydrophytes. In spite of the fact that there is a difference between desert plants and terrestrial plants in general, it is not likely that there is a large difference between an ordinary leaf and a succulent one for the following reason. The essential process of assimilation is going on in the mesoderm on an atomic scale, while the constructional differences between the ordinary and the succulent leaf are, in comparison, on a macro scale. Furthermore there are no typical differences in the anatomy of submersed plants living in stagnant and non-stagnant water. This is contrary to expectations, if it is remembered that one of the most obvious results of the present investigation is that such differences are typical. Therefore I have rejected this hypothesis, and it is assumed that the assimilation rates do not vary very much for different plants species ; always allowing for a systematic difference between ordinary terrestrial plants and submersed ones, and perhaps for gymnosperms in comparison to other plants. The second possibility is that this systematic difference in assimilation rates is large and that the observed isotope effects depend on the completeness of the assimilation. A one-step rate process proceeds best with incomplete reactions ; i.e. the isotope effect will be maximum if the favoured molecules are drawn from material that is continously being replaced with fresh material. If the reaction is complete there will be no enrichment at all. Consequently it must be concluded that according to this theory the most favourable places for enrichment are deserts and other windy places and the most unfavourable surroundings tropical rainforests, etc. Using the same argument it can be shown that the enrichment observed for submersed plants in stagnant water should be less than that for plants living in non-stagnant water. A glance at Figs. 1 and 2 shows the incorrectness of these conclusions. Consequently we are forced to investigate whether the cyclic exchange of carbon dioxide already discussed in the previous paragraph might explain the observed
251
v&es. For &re&ti& ph&s the situafkn can be described in the foilowing wrzy (Fig, 3). Carbon dioxide is assimilated by the plant from the local air with slightly different reaotion rates for PO1 and c”*Qr, thenatored in the plant for some time and eventually r&urning to the air from the
of the n&r&ganisms.
I
DESCRY”
1
aar
I
90.0
EMERGEN?
A11 the time
HYDROPWYTES~
PLANTS
f
90.5
I
91.0
c ‘s&r Fig. I.
Fig. 3.
there is an ex&ange of c&xm dioxide between t&e b& la;ndthe main ~trn~sphe~~ These ~n~tj~~ are e~~a~~nt to thsaa used in cy&c isotope ~~~rne~t processes. According to this theory the enrichment will be smaJh3stwhere the “soil respiration” is negligible and where the “local atmcq.&ere ” for some rewon or other doers not develop, i.e. in a desert OT at a ~~~ntiy windy place. The ‘krgest isotope
Variation in the relativeabundanceof the car&m ieotopea in plants
effect will be observed where the cyclic process is most intense, e.g. a tropical rainforest. This is in accordance with the observations as can be men from Fig. 1. The four lowest values observed in the main series of terrestrial plants (90690.6) are from plants which have grown at notoriously windy places (24, 33, 71 and 101). In the sea and in lakes and rivers the cyclic process will develop in stagnant water (Fig. 4), but not normally in non-stagnant. This is also in accordance with the observations. If there is a supply of carbon dioxide orig~ting from limestone, the enrichment normally will be smaller, because the ratios observed for limestones are mostly around 89 or somewhat lower. The influence of this source varies in accordance with local conditions. This point has not been investigated, but there is no reason to doubt the reliability of this conclusion. Probably some of the author’s plant values are influenced by this factor, ATMOSPHERE but it is impossible to prove anything without a thorough knowledge of the exact place c;o;G;zGzT1__t__ where the plants have grown I WATER -4 L--e-_ 1_c__-It might also be expected that the enrichment will vary with the height from the ground in a biotope, being largest close to Fig.4. the ground and smallest at the tops of high trees. The reason for this is, of course, that the exchange with the main atmosphere by winds will be largest at the tops of high trees. Also, the enrichment will not be constant in space and time because the conditions will vary from place to place and from season to season. An essential point in this type of enrichment is that the cycle should not be quite complete, but that there should always be an exchange with the bulk of the atmosphere or sea-water. Without this exchange the enrichment will stop. The observed variations in the ratio are not very large, but the variations will be accentuated for the heavy isotope C-14. It is very likely that in the future these cyclic enrichment factors have to be taken into account. Especially dangerous is, of course, contamination with “fossil carbon dioxide” which is free from radioactivity [lo]. The possibilities of investigating the history of early life on earth are of course somewhat modified by the results of the present investigation. On the other hand, it’ seems most natural to assume that life was first created in stagnant water, and if this hypothesis is correct there is a fairly good chance of tracing life far back into pi-C&mbrian times. SUMMARY AND GENERAL CONCLUSIOXS fn the preceding paragraphs it has been shown that enrichment of the light carbon isotope in plants, which was discovered by NIER, is intimately connected with the cycle of carbon dioxide. This explains why in places where the cycle cannot develop, e.g. in the open sea or in deserts, enrichment is much less than in places where the c:ycle is more complete and intense, e.g. in tropical rain-forests or saint water.
253
The v~~i~tio~ in the isotope ratio of carbon is thus not, primarily a problem of sy~~tie boteny but of eoolugy. In order to study tke influence of tbe various factors in u~ural s~~n~~, e~olo~ snd ~h~~~~~~ pmbabfy have to coopen&t. Thiri 1’~eqecdalfy impttrtant, in ~sti~g the observed anon&y uf ~noSperms.
The question immedi&ely arises of wh& is happening to the plant isotope r&io when it is trausferred to the animal kingdom. Will the ratio change in the animal body or not ? At present I am investig&ng some typic& aspects of this problem. It is also inertia to apeoul&e about the ~~ib~ties of ogling variation in the ratios of other sable elements. It is obvious that the chances for enriohment increase if there is s oyelic process in operation. But in order to obtain a! large isotope effect it is very impotent that the smonnt of m&erial of an element taking part in a cycle is not large and that the cycle is repe&ed rapidly. This is not the ease in moat cyclic processes in the earth’s crust. ~he~ore there must be an exchange of m~~ri&l with a major sou~ee of the element. This means that it is probably nitrogen which, besides carbon, oxygen and hydrogen is the most fatvourable ease, assuming of course that there is & difference in the reaction rates of the nitrogen bacteria. In the main, however, the favourable circumstances met with in the case of carbon must be rare, ~e~~e~e~-Th~ presetit inve~igat~on has been supported by a grant. from Statens ~~~~~e~~~~~ ~~8~~~~~” Not being 8 botanist myself I h&ve been privileged to receive help and advice in the selection of suitible species from my colleagues et the Bot&cal ~~~rn~~~ of the ~~~~~~, Prof. 3% &XTh, Prof. 0. H. SYB~JXINC), Dr. E, ASPLUXB,Dr. S, AHLXZZ~ and Dr. H. RUBN af Rantaien.
[If NRC% A. 0. and GSYLW~A.N~~N, E. A.; V&&ions in the relative abundance of the o&rbon ieti~es. J. Amer. Chem. 800. 1939 61 697, [2] M--Y, B. F. md NXBB, A. 0.; Variations in the relative 8bundance of the carbon iwtopee. Phys. Rev. 1941 lie 771. (31 RMTXAXA, K.; A note on the original lQ48 QI 189. 143 W~CKBMN, F. E., Bzxx, R. isotopic composition of terr&ri&l carbon. J. Ml. of the carbon isotopes in and YON UBISCS, If.; On the variations in the relative abuz&nee csrbonate mirier&s, 3, Ueoi. lSBf8@ 142. fb] W~GXXAX, F. E. 8nd vex Uznsca, H.; Two no* on the iwtopic co~t~t~tio~ of carbon in miner&. &so&m. et Coamochim. Acta 1951 1 1 IQ. fQ] vaN ECEERinvwtigxtion into the isotopio compoWAX?% H., ~0~4 thmc~, ff, and WICKMAN, F. R.; A pdiminary sition of carknm frcun some a&&he intruhna. Geocb, et f2ussmochim.Acte 19.52 E 207. [7f VON Foooa, J.; Wygieniwhe ~~~~~h~~~ iibw Luft, B&en und Waster. ~~un~hw~~ 1881-1882. [8] STEWART,D. W.; Isotopes. Anma Rev. of Phys, Ffiem. 19sf% 67, [S] Wsxs, J. W.; The r&t&+ of ~ho~~th~~ to reepiration. Doctors1 && Univ. of C&f,, Berkeley 1949. [ro] JFUNT,R. F. 8nd I~EVEY jr., E. S.; gibbon dating of ~~-~~~~e~~ eventa. Amer. J. Sci. 1961 %@- .26X ill] LAXDEWIWN,S. and MARVEL, A.; On the rtktive abundance of the carbon isotopes in Swedi&h alum shales. Geochim. et Cosmochim. Acte. In Preae.
Var~a~ons in the relative abunda~e~ of the carbon isoto~s in plants* FRANS E. WICKMAN Riksmuseet,
Stockholm 50, Sweden
(Received 21 January
1952)
ABSTRACT The cl*/@ ratio of 105 plants mpmaenting 811the major system8tic groups has been dekmined. Except perhaps for gymnosperms there are in principle no systematic differences between the groups. Charscteristic differences occur, however, between plantsgrown in different biotopes, and these differences sre related to the varying intensity of the local carbon-dioxide cycle.
INTRODrrC!cIOW A. 0. NIER and his co-workers [l], [2] have shown that the isotopic composition of carbon in living matter and related materials is different from that in carbonates. So far the number of investigated plants is small, and in a compilation made by K. RANEAMA[3] in 1948 only seven examples of present day plants are presented. This material is too limited to be used as a starting-point for geochemical calculations of the circulation of carbon in nature, and in an effort to fill this gap in our knowledge the pr&ent investi~tion was started. THE MATERIAL The material consisted of plants from the herbarium of the Riksmuseum in Stockholm which had been preserved for periods of time varying between 1 and 115 years. However, this circumstance seems to have no influence on the results, judging from the fact that these do not vary s~tematically with the “herbarium age ” of the plant. This is not surprising if it is remembered that the preparation of a plant for a herbarium is merely s, drying process. The plants were burned with oxygen in a combustion furnace by A. PARVEL using the s&me technique as described by S. LANDEBUREN and A. PARVEL[ll]. Those plants con~i~ng calcium carbonate, e.g. Chara, were treated witn acid before being burned in order to avoid contamination from occluded calcium carbonate, The mass spectrometric measurements were performed by R. RYHAGE at the Department of Chemistry of the Karolinska Institut. The reproducibility of the measurements is within Ifr O-1 unit, in most cases within about &I*05 unit. The results are referred to the same standard sample used in the earlier papers of this series [4], [ci], f6]. Originally the intention was to have common representatives of all the major plant groups. Furthermore, the same species was to be represented by plants grown in very different surroundings, e.g. plants from the Northern and Southern limits of their distribution. The results obtained were so in~resti~~, however, that the material had to be completed using ecological instead of systematic viewpoints. They are presented in Table 1. *
Paper No. 5 in a series devoted to the application of isotope ratios to geological problems.
17 Oeochim. Vol. 2
243
Abbreviatkww;
m = marine;
NO.
1
2
-.
!&bk 1 d = desart plant; 1 = laoustrine;
-I_____.--
tr = tropical rain forest plant
Nome and toudity
C’yY
Ulva lactuca, Malmo, Sweden. . . . . . . . . . . . . . . , . 171va lactuca, f. &.&b, Venice, Italy . . . . . . . . . . . .
III III
Charoph~sae Ivetofta, Sk&me, Sweden . . . . . . . . . . . Uhuruf&i&, Sah, Argentine . . . . . . . . . . . . = . _ Uiboro fr&l&, Lake Ringsjiin, Sweden . . , . . . . _ . . . HI i%sra jzcbata, “Par%teiner See,” A~errn~~de, Germany. . . . Okra ~~~~a, ground, Sweden . . r , . . . _ . . . . . 7 3
Ohara crilaita,
8
Fuctba fur&us,
9
Bk.tw o~esimloeus,Varberg,
10 11 12
.
m
. . .
1 1 1 ni
_
f. vatiiEi8,
Sitka, Ah&s, , . . . . . . . . . . Sweden . . . . . . . . . . . . . . between St. Paul and Amsterdam, Atlantic
Macracy&s pyrifera, Ooean * . a . . . . . . . . . . . . . . . . . . . . . . . &wgamm gMu!&a.efoEium, Sidney, New South Wale8 . . . . Sargawum nakz?as, Sargasso Sea, Atlantic Ocean . . . . . . . . Rhodophweae i&spue, Eristineberg, Bohm&&n, Sweden . f . . . 1 . Cho9&-as m&p8, Digby Neck, Nova, Scotia . . . . . . _ . . .
13 14
~butrus
17 18 19 20 21
&brchau& Marchantia Xarcha&.a, Plagioahika Pkgiochila
22 23 24 25 26
Hy~~~rn 8~~~~6, Ryd, V&8tergothmd, Sweden . . dioEdorpn e&y&, Rydboholm, Uppl~nd, Sweden. . . . . Sp~~rn f~~~~~, Fiord0 Martine8, Bahia Pliischow, upturn ~rg~oh~~~, Ydre, Sweden . . . . . . _ . . Sp&r~m, Taemania I . . . . . . , . . . . . . . .
27 23 29 30
Ptem’doph~tu 1. Lycopodinme Lycopodaum selego, Caldas, Minas Geraes, Braeil . . Lycopo&um s&go, Restock, Dalsland, Sweden . . Sekxginella sekaginoides, Forssa, Hiilsingland, Sweden Se&&elk selagi,noides, Canada . . . I , . .
31 32 33
Ugathea aMra&s, Atherton Tableland, N. Queer&and . ~ _ . . Bryopteris the~yp~, Danderyd, Sweden . . . . . . . . . . . Bryvpterie t~~~~, SE side of Hibmanjaro, Eitet Africa _ . .
borteroana, Puyehue, Osorno, Chile , , , polymorpha, Halltorp, SmAlland, Sweden Tasmania . . , . . . . . . . . . . . aepEenioides, Hjnleerud, Sweden . . . . cava. Caldas, Minas Gerabs, Bra4 . . .
89.37 90.30 90-03 9043 9043
m m Ill
m nl
III III
. . . . _ . . . . . . . . . . . , ,
. . . . . . . . . . . .
2. Nusci
244
. . . . . . Chile . . .
. f
. .
. _ . .
. . . ‘. . . . . . . . . . . . _ . . . . .
. . . . . . .
90.76 90% 00.55 90-96 91.37
Nb79 9143 90.72 90.84
90.96 90.99
90*5x
Variations in the relative abnndence of the arbon
isotopes in planta
Table 1. (Continued) Name
No.
and
T
locality
O’/Q’
-7
Phanewganuw A. Bymnospermm 1. cyeudinut?
34
Uya~
me&u, Darwin, N. Terr., Australia
. . . . . . . . . . . .
90.48
36
2. (3inkgoim.e aiinkgo biloba,Kiangsi,mina . . . . . . . . . . . . . . . . .
90.70
36 37 38 39 40 41 42
A~azccaria angu&folicl, Rio Grande do Sul, Brazil . . . . . . Araucati biramdata, New Caledonia . . . . , . . . . . . . P&a abkx, T&by, Uppland, Sweden . . . . . . . . . . . . Pieeta e8perat4, Radja and Yellow River gorges, Eastern Tibet Pinru, silve8tri8, NW of Troizkosavsk, Transbaikalia . . . . . Podocarpue gradion, Kirstenbosch, Cape Province, S. Africa Podocar~s totara, Waitakera Hills, North Island, New Zealand
3. Cmiftxw . .
. . . . . .
90.62 90.49 90.67 90.80 90.64 90.62 90.63
. . . . . .
Be Angiospermae a) Dictyledoneae
43 44 46
1. Polycarpicae Brosenia 8ehrebev-i. Fish Lake, Chisago Co., Minn., U.S.A. . . Trigynaea eeua&ren8& between Tena and Napo, Prov. Napo stasa, Ecuador . . . . . . . . . . . . . . . . . . . . . Vdrola paponie, Tingo Maria, Prov. Hu&nuco. Peru . . . . .
1
89.26
. . . .
tr tr
91.27 90.88
Ck&gonurn acadhopterum, var. eetosa, between Annaju and Gnaurs, Askhabad. . . . . . . . . . . . . . . . . . . . . . . . . .
d
89.63
d d d
89.66 89.66 89.69 90.87 90.81
. . Pa-
2. Polygon&8
46
3. ccntroqi?lwl&?
47 48 49 60 61
Arthrophytum wborerrcenu, Repetek, Merv, Ealoxylon aphylLum, Central Asia . . . &duoh richteri, Repetek, Transcaspia . . Nd.lati media, LjusterS, Sweden . . . Stellaria media, Misserghin, Algeria . . .
62 63
kda cym.osa, Iquitos, Dep. Loreto, Peru . . . . . . . . . . . Tamariz androeetii, Amu-Darya, Turkestan . . . . . . . . . .
tr d
91.09 90.71
64 66
ChTy8odbkZmy8 weberbaueri, Tingo Maria, Dep. Huanuco, Peru . . . Dipterocarpus akztus, near Calcutta, Bengalia, India . . . . . . .
tr
91.12 90.72
66 67 68
Aetragalu8 pauci jugtu, Uch-A j ji, Transcaspia . . . . . . . . . . . Entadopeis polyphytla. Iquitos, Dep. Loreto, Peru . . . . . . . . Sckrolobium, !i”ingo Maria,Dep. Hu$nuco, Peru . . . . . . . . .
d tr tr
90.66 91.12 90.71
1
90.30
Transcaspia
. . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . _ . . .
. . . . . . . . . . . .
4. Parietake
6.
‘7.
Ro8lde8
hdQ8tGmod48
Poddemum ceratophyllum, on rocks, St. Regis River, Hogansburg, FranklinCo.,N.Y.. . . . . . . . . . . . . . . . . . . . .
245
.L
60 61 62 63 64 66 66 67
8. Nyrtales sne%dora, Warrumbungle Rsngee, New South Wales I Emzlyptw pol~lonthemos,Canbma, Auetrdia . , . . . . . . . Eugmia buxifolia, Key West, Florida, U.S.A. . . . . . . . . . . Eugenia mdcrophylla,Lantao I&nd, Kwangtung, China . . , . &tr~adderoe ongdijolia, Bosch Kloof, South Africa . . . . , . . 4%kOeidslroe poiyneorpha, subep. iwna, Huehue, Island of Hawaii. ~~hy~~ mm%eiWum, Atvidaberg, Sweden . . . . . . . . . Hippsti ~~T~~~ Friggesund at River Svhga,H~~~gl~nd, Sweden Mypius
1 1
9. Fagales 68 69 70 71 72 73
Bet&, %&&ad, Sweden . . . . . , . . . . . . . . . . . I s B&&Z emmi, Petropaviovak, Kamtchatka, twig. . . . . . . ~ . B&&b emnuni, Petropavlovsk, Kamtehatka, leaf . . . . . . . . .
9tm’J 9144 90.90 90.56 90.70 9WR7
Punta Arenaa, Patagonia. . . . . . . I . . Djebel’Ballota, Tunis . . . . . . . . . . . . . . . QWTW robw, Riainge, tistergfitland, Sweden . . . . . . . . . I
Nothofague
t&emu
bstuloidae
ikz,
10.
micalea
74 76
F&M paraw&, Quietocecba, Iquitos, Dep. Loreto, Peru . . ~ . . 0lmedi.a aepwa, Tingo Maria, Dep. Hu$nueo, Peru . . . . ~ . . .
76 77
Pr&a
78
Pierolemmo
79 80
Cork wdosa, Tingo Maria, Dep. Wu&nn\leo, Peru . . . . . . . . Jacaw~.& copaia, Tingo Maria, Dep. Hu4nuc0, Peru , . . . . . .
81
Sommera sabicsoides, Hacienda Sale&d, fquitoa, Dep. Loreto, Peru
82
Aobd& acne,
tr tr
11. Pro&.?&% ~y~~~~
.Proi+s ~~~,
&x&e B&en, Eritrea . . . . . . . m . . . . ~
Karoo Poort, South Africa
. . . . . . . . . .
12. Terebintak 8~rtccci,
Iquitos, Rep.
hF&O,
Peru
. . . * . . . . .
tr
914%
13. Tubiflorw t,r t#r
14. Rrbiales
15. CampcsnautcPtae Lake L&j& Vrena, S~de~an~nd,
Sweden .
tr
91.27
I
90.74
bf Monocotyledoneae 1. HeMiae Butamue umbeU.atuu,Lake Kolbotten, Naeka, Sweden. . . . . ~ I 83 Flottiund, Uppsala, Sweden . . . . . . . . . 84 i?Boda m&is, . . I . sz5 VaUisneria am&cam, Farleip Point, Cayuga Lake, N. Y.
9OM 90.2’; R9.9 1
2. P0tamo@mbale8
Naj@a mc;cr&wl, Laduviken, Stockholm, Sweden. h&mwpton dclwns, Irrigation e&m&l,Domoecua, by& : : : : Pdwwgs&m wfa~~, Eneta damm, G-amla Up@, Sweden . . l”o~ pectisauttae,the Sea S of Ski@nge, 8kkt5, Sweden Pofsmopb poEygosw, Ciddaa, Mkiss Gtyriss, Brazil . . . . . 91 Zoebpa III4pjwQ.Buccaritta, Fiume . . . . . . . . . . . . . 9% ZfMera 9ntwinu, v. a~~fo~, Styrraii,Bohuaiiin, Sweden. . .
a4 87 88 89 90
246
: 1 I .
. 1
I
90.18 90.85
1
90+51 89.47 9Im 89-W
1
. . .
111
. . j
m
I : ’
1 m
/
1 89.32
Variations
in the relative abundance of the carbon isotopes in plants Table I. ~co?i,f~~~~~
I
iName and Eocolity
No. -_
-1
.-
3. Pritipee
I
tr
90-89
tr
91.39
. . . . . . . . . Wolff&z urrhiza, St&~&nt water at Dunaharaszt~, Danube, Rounl%nia
1 1
91.04 90.88
6. Parve Typhu anguatifotia, Lake Normjon, Bladitker, Uppland,
. .
1
9036
Laaeiaeis ligulaia, San Juan, Iquitos, Dep. Loreto, Peru . . . . . . Paspalum distichwm, Stanford Univ. Lake, Santa Clara Co., Cal, U.S.A. 100 Paepalum diatichwm, Fiscbhoek, Cape Peninsula, South Africa . . .
tr 1 1
93
Degnboncu.s prunifer,
Jquitos, Dep. Loreto,
Peru
. . . . . . . . .
.
94
95 96
97
4. Synanthue Carludovica palm&a, Hacienda Clementina on Rio Pita, Prov. LOS Rioa, Peru . . . . . . . . . . . . . , . . . . . . . . . . .
5. Spathiflorae Lemna minor, M&ls&ker, S~dermanland, Sweden
Sweden
98 99
8. Gypera& 101 Carex 102 103
Andes NW of San Juan, North Argentine . . . . Carex Leporina, Kiisna, Bohusliin, Sweden . . . . -. . . . . , . . Dipbsia kar~t~~ol~a, Tingo Maria, Dep. HuBnuco, Peru . . . . . .
tr
9059 90.79 91.24
tr
90.64
~RCUTW,
9. gr~~~8 104
acne edwtrdi. Hacienda C~e~ent~na on Rio Pita, Prov. Los Rioe, Peru . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10. Liliijl4m.M 105
Eichkornia erassipes, in the swamp *‘La Siganea,” Catelina, Pinar de1 Rio, Cuba . . . . . . . . . , . . . . . . . . . . . . . .
90.91
I
L.
i
PRELIMINARY DISCUSSION OF THE RESULTS
The results of ‘NUB and his co-workers indicebtedthat there might be large variations in the CY/CY ratio of plants, and Table 1 is & confirmation of their results. There are several examples of the same species from two different localities, but they do not show any definite relatio~hip between isotope ratio and latitude, as can be seen from Table 2. It might therefore be conelnded that the ambient temperature is of no primary importance. On the ether hand if the material is divided into several groups such as marine plants, limnic plants, terrestrial plants from tropical rain-forests, desert plants, and other terrestrial plants, the distribution shown in Fig. 1 will be obtained. From this figure it is quite evident that some of the groups are quite homogeneous, especially marine plants, tropical rain-forest trees, rendthe group “other terrestrial plants.” If this lest-mentioned group is divided into three main subgroups : angiosperms, gymnosperm8 and cryptogames, it is interesting to note that two of the three groups show almost identical distribution, but that the third one, i.e. gymnosperms, sys~m~ti~lly gives somewhat lower ratios. Whether this trend is real or is due only to an u~avourable selection of plants, is impossible to determine with 247
F.E. WICICMAH
LOCddy
Plant d?pe&?
Italy ........... Sweden .........
45” lG 5P .K
Nova Scotia . . . . . . . Sweden. . . . = . . . . .
4P N 6O"N 5PN 59 "K 20" Y 60"h' 50"fX 60"N
Bring&o&a, Sweden Mariefred, Sweden. Brazil 1 _ . . . . Sweden . . . . . Canada . . . . . . Sweden . . . . . East Africa. SWedSXl
.
. . . ~ 1 .
. . . _ _ .
. . . . . .
. I . . . .
. . . . . . . .
.
s
.
.
.
.
.
Algeria. _ _ . . . . . . . Swe&x3 * : . . . . . . . California ........ South Africa .......
:
:
5O s 60'N 35"E 60°N
'
35ON 35"s
any degree of certainty from the limited material so far studied, but it may quite well be that this trend really exists. The desert plants show two wee-defied groups of values. It is in~res~ing to note that the 89*6-group grew in real deserts, the 9006-group in one case close to a river, in the other at a railway station. The limnic plants form a very heterogeneous group. It consists of (a) @ants which are rooted at the bottom and raised into the air at the top, and fb) submerged hydrophytes which live in deeper water. The emergent hydrophytes usually contain less chloiophyll in the submerged portion than in the portion above water. We may regard the floating hy~o~h~s, which are r&ted to the bottom but float their foliage upon the surface of the water, as a transition stage between these two groups. In all three cases the water in which the plants live may be stagnant or not. In Table 3 the limnic plants have been ciaasified according to the a~ve-mentioned properties, and an inspection of this table shows that isotope ratios around 91 are found far all plants living in stagnant water. On the other hand most submerged plants living in non-stagnant water give vaiues under 9@6, and the emergent hydrophytes elm form an i~omogen~~ group (Fig, 2). Before discus&g these results it might be profitable to recapitulate a few facts about the local carbon dioxide cycle. TEE
CYCLE OF CARBON
WITH SPECIAL REFEBEXWE TO
PLANTS
For over a hundred years the cycle of carbon in nature haa been studied by practically all hinds of soientists, and it is now known that it consists of a series of smaller cycles for~g a rather intrkate system. 248
Variations in the relative abundance of the esrbon isotopes in plsnts Table 3 Name
1
2
f e B 8 5 f 6 e/s f 6 6 8
ns ns ns n6 n8 6 n5 sjns (8) nu 6 n8 ns ni3 6 ns 6 sjns ns 8
C’fp
_-. 43 83 4 5 6
105 84 67 95 82 66 86 99, 100 59 87 88 90 97 85 96
Brasenia schreberi ............ Butomus umbelbtus ........... Chara foetida ............... Chara fragilis .............. Chara $~bata ............... Eichhoka crassipes ........... Eloeda eanudensis ............ EippwG ~~aT~8 ............ &mm rn~~. ............. ~bel~a ................ ~~ophyll,um ve~~~~t~v~ ........ Najas marina. ............. Paspalum distiehum ........... Podostemum ceratophyllum ........ Potamogeton densus ........... Potamogeton natans ........... Potamogeton pol ygonus .......... Typha anguatifolia ........... Vallisneria americana .......... Wolffia arrhiza .............
(:I 6 f 8 e 8 f
89.25 90.86 90.30 90.03 90.03 90-91 90.2i 91-01 91-04 90-74 91.16 90.18 89.51, 89.53 90.30 90.85 90.51 91.05 90.86 89.91 90.88
1. e = emergent hydrophyte; f = floating hydrophyte; 8 = submersed hydrophyte. 2. 6 = living in stagnant water; ns = living in non-stagnant water. i
In the present: paper we are concerned only with plants and therefore all other aspects of the carbon cycle will be neglected. The terrestrial plants obtain their carbon dioxide from the air, the mean content, of which is about O-03 ~01% . Depending on local factors which hardly can be account ed for in all specific cases, large variations around this mean value have been observed. However, some regularities have been noticed which are of special interest in connection with the carbon-dioxide fixation by plants. VON FODOR in 1881 was the first to observe that there is a daily periodicity in the CO, content of air, the maximum occuring during the night and the minimum during day time. This pronounced effect shows that the mixing between the main atmospheric air and the air layers close to the ground is not i~tan~neous, i.e. that diffusion is a slow process. It is also well-known that the air layer in immediate contact with the soil is enriched in carbon dioxide. The reason for this is that the soil produces carbon dioxide partly by the respiration of the microorganisms in the soil itself and partly by the respiration of the plant roots. There seems to be general agreement among botanists that the assimilation and production of carbon dioxide in a forest or other biotope are normally in equilibrium with each other. The soil, the atmosphere and the plants constitute the participants of the local cycle of carbon which is characteristic of plant life. Of course, their relative importance varies according to local conditions. Of great interest in this cycle is its completeness, i.e. to what degree the soil carbon-dioxide is directly assimilated by the plants. It is obvious from what has been said above that this process is 249
more complete if the plants are low-grown and live in an area under lee, especially if the carbon-dioxide produotion of the soil is high. On the other hand if a plant lives isolated from other plants in a windy place on an oceanic island, or in sand without muoh soil, it will generally obtain practically all of its carbon-dioxide supply from the main atmospheric air. These two examples are extreme c&8es,end 8s a rule conditions are somewhere in-between. Probabljt the first case will be most closely realized in a tropical rainforest, and the second in a desert. For hydrophytes there are several cases which should be discussed separately. First of all there are the emergent hydrophytes which are rooted to the bottom of the lake or the sea, but assimilate mainly atmospheric carbon dioxide. In most respeots they are equivalent to terrestrial plants, except for one thing which will be discussed below. The second group consists of submersed plants and the third of floatiug hydrophytes. This third group, to which e.g. water-lilies belong, are probably ~1-1~ related to the second one, because they do not extend to any height above the water surfaoe, and it might confidently be assumed that the carbon dioxide content of a very thin byer close to the water surface will be determined by the oarbon dioxide of the water. The submersed plants obtain their supply of carbon dioxide from the water. As is well-known, water contains carbonate ions, bicarbonate ions and dissolved carbon dioxide gas. There hresbeen much discussion among botanists and physiologiets ae to whether the plants a&milate the gas exclusively, or whether they are able to uee tbe ions directly. For the present discussion this point ia not important, since we &re primarily interested in isotope ratios which will not vary on account of the exobange of carbon stems between the different molecules and/ions. The total content of carbon dioxide in sea water varies greatly, but a normal value ia about 0.6 ~01%) i.e. the concentration is about ten times &s high as in the etmosphere. In lakes and rivers the content is also greatly variable, but for pure water in oor@ot with air the content is about 0.03 vol%, which means that it is the mrne as in air. ‘If the partial pressure of carbon dioxide is higher the amount of gas in the water will be lerger, and the same is true if the water is buffered by the .preaence of carbonates. In the open sea the carbon dioxide, produced at the bottom by microorganisms and by the reepiration of plants and eninarrle,will not have the same possibility to influence dire&y the clssimilation of submersed and emergent plants partly on socount of the &u&&ion of water by currents and partly on the high content of carbon dioxide present in se& water. However in a small stagnant part of the sea or lake or in a small pond, the conditions for a submersed plant will be almost the Borne as for a terrestrial plant. There will be an exchange of carbon dioxide with the atmosphere, and perhap also by convection currents with the main part, of the water beain. Finally there will be a supply of carbon dioxide with the groundwater, and this source might be of speaial importance in the ~888 of small springwater lakes without influx. If limestone is present in the area where the plant is living some of the rtssimilated carbon dioxide might derive from diaintegmted or dissolved rock material. The importance of this factor will of course vary oonsidembly according to local oircumtinces. 250
Variationsin the relativeabundanceof the carbonisot.opes in plants DISCUSSION OF THE RESULTS WITH SPECUL REFERENCE TO THE CYCLE OF CARBON DIOXIDE According to a statement of WEIGL [9] (cited after [S]) the assimilation rate of @‘O, is about 17 % less than that of C?O,. Probably this would correspond to a value somewhat around 5 % in the case of CY30,, which is a very serious discrepancy if one remembers that the pzaximum enrichment found in the present investigation is about 2 % . WEIQLB experiments are, however, very difficult to perform, on account of the simultaneous respiration and reassimilation of carbon dioxide by the plant, and his results cannot therefore be regarded as conclusive. The results of the present and earlier measurements on plants confirm, however, the reality of such a difference in the assimilation rates of the carbon dioxide molecules, but the observed effects are small. It might be asked whether the difference in the assimilation rates is alone responsible for the complete enrichment (one-step process), or whether the cycle of carbon dioxide, too, is essential in order to obtain the observed enrichments (cyclic process). Assuming the first alternative to be correct there are two possible theories. First, it might be thought that the difference in assimilation rates varies from species to species, or perhaps from plant to plant. Large differences should then be expected between e.g. ordinary plants, and xerophytes, and especially hydrophytes. In spite of the fact that there is a difference between desert plants and terrestrial plants in general, it is not likely that there is a large difference between an ordinary leaf and a succulent one for the following reason. The essential process of assimilation is going on in the mesoderm on an atomic scale, while the constructional differences between the ordinary and the succulent leaf are, in comparison, on a macro scale. Furthermore there are no typical differences in the anatomy of submersed plants living in stagnant and non-stagnant water. This is contrary to expectations, if it is remembered that one of the most obvious results of the present investigation is that such differences are typical. Therefore I have rejected this hypothesis, and it is assumed that the assimilation rates do not vary very much for different plants species ; always allowing for a systematic difference between ordinary terrestrial plants and submersed ones, and perhaps for gymnosperms in comparison to other plants. The second possibility is that this systematic difference in assimilation rates is large and that the observed isotope effects depend on the completeness of the assimilation. A one-step rate process proceeds best with incomplete reactions ; i.e. the isotope effect will be maximum if the favoured molecules are drawn from material that is continously being replaced with fresh material. If the reaction is complete there will be no enrichment at all. Consequently it must be concluded that according to this theory the most favourable places for enrichment are deserts and other windy places and the most unfavourable surroundings tropical rainforests, etc. Using the same argument it can be shown that the enrichment observed for submersed plants in stagnant water should be less than that for plants living in non-stagnant water. A glance at Figs. 1 and 2 shows the incorrectness of these conclusions. Consequently we are forced to investigate whether the cyclic exchange of carbon dioxide already discussed in the previous paragraph might explain the observed
251
v&es. For &re&ti& ph&s the situafkn can be described in the foilowing wrzy (Fig, 3). Carbon dioxide is assimilated by the plant from the local air with slightly different reaotion rates for PO1 and c”*Qr, thenatored in the plant for some time and eventually r&urning to the air from the
of the n&r&ganisms.
I
DESCRY”
1
aar
I
90.0
EMERGEN?
A11 the time
HYDROPWYTES~
PLANTS
f
90.5
I
91.0
c ‘s&r Fig. I.
Fig. 3.
there is an ex&ange of c&xm dioxide between t&e b& la;ndthe main ~trn~sphe~~ These ~n~tj~~ are e~~a~~nt to thsaa used in cy&c isotope ~~~rne~t processes. According to this theory the enrichment will be smaJh3stwhere the “soil respiration” is negligible and where the “local atmcq.&ere ” for some rewon or other doers not develop, i.e. in a desert OT at a ~~~ntiy windy place. The ‘krgest isotope
Variation in the relativeabundanceof the car&m ieotopea in plants
effect will be observed where the cyclic process is most intense, e.g. a tropical rainforest. This is in accordance with the observations as can be men from Fig. 1. The four lowest values observed in the main series of terrestrial plants (90690.6) are from plants which have grown at notoriously windy places (24, 33, 71 and 101). In the sea and in lakes and rivers the cyclic process will develop in stagnant water (Fig. 4), but not normally in non-stagnant. This is also in accordance with the observations. If there is a supply of carbon dioxide orig~ting from limestone, the enrichment normally will be smaller, because the ratios observed for limestones are mostly around 89 or somewhat lower. The influence of this source varies in accordance with local conditions. This point has not been investigated, but there is no reason to doubt the reliability of this conclusion. Probably some of the author’s plant values are influenced by this factor, ATMOSPHERE but it is impossible to prove anything without a thorough knowledge of the exact place c;o;G;zGzT1__t__ where the plants have grown I WATER -4 L--e-_ 1_c__-It might also be expected that the enrichment will vary with the height from the ground in a biotope, being largest close to Fig.4. the ground and smallest at the tops of high trees. The reason for this is, of course, that the exchange with the main atmosphere by winds will be largest at the tops of high trees. Also, the enrichment will not be constant in space and time because the conditions will vary from place to place and from season to season. An essential point in this type of enrichment is that the cycle should not be quite complete, but that there should always be an exchange with the bulk of the atmosphere or sea-water. Without this exchange the enrichment will stop. The observed variations in the ratio are not very large, but the variations will be accentuated for the heavy isotope C-14. It is very likely that in the future these cyclic enrichment factors have to be taken into account. Especially dangerous is, of course, contamination with “fossil carbon dioxide” which is free from radioactivity [lo]. The possibilities of investigating the history of early life on earth are of course somewhat modified by the results of the present investigation. On the other hand, it’ seems most natural to assume that life was first created in stagnant water, and if this hypothesis is correct there is a fairly good chance of tracing life far back into pi-C&mbrian times. SUMMARY AND GENERAL CONCLUSIOXS fn the preceding paragraphs it has been shown that enrichment of the light carbon isotope in plants, which was discovered by NIER, is intimately connected with the cycle of carbon dioxide. This explains why in places where the cycle cannot develop, e.g. in the open sea or in deserts, enrichment is much less than in places where the c:ycle is more complete and intense, e.g. in tropical rain-forests or saint water.
253
The v~~i~tio~ in the isotope ratio of carbon is thus not, primarily a problem of sy~~tie boteny but of eoolugy. In order to study tke influence of tbe various factors in u~ural s~~n~~, e~olo~ snd ~h~~~~~~ pmbabfy have to coopen&t. Thiri 1’~eqecdalfy impttrtant, in ~sti~g the observed anon&y uf ~noSperms.
The question immedi&ely arises of wh& is happening to the plant isotope r&io when it is trausferred to the animal kingdom. Will the ratio change in the animal body or not ? At present I am investig&ng some typic& aspects of this problem. It is also inertia to apeoul&e about the ~~ib~ties of ogling variation in the ratios of other sable elements. It is obvious that the chances for enriohment increase if there is s oyelic process in operation. But in order to obtain a! large isotope effect it is very impotent that the smonnt of m&erial of an element taking part in a cycle is not large and that the cycle is repe&ed rapidly. This is not the ease in moat cyclic processes in the earth’s crust. ~he~ore there must be an exchange of m~~ri&l with a major sou~ee of the element. This means that it is probably nitrogen which, besides carbon, oxygen and hydrogen is the most fatvourable ease, assuming of course that there is & difference in the reaction rates of the nitrogen bacteria. In the main, however, the favourable circumstances met with in the case of carbon must be rare, ~e~~e~e~-Th~ presetit inve~igat~on has been supported by a grant. from Statens ~~~~~e~~~~~ ~~8~~~~~” Not being 8 botanist myself I h&ve been privileged to receive help and advice in the selection of suitible species from my colleagues et the Bot&cal ~~~rn~~~ of the ~~~~~~, Prof. 3% &XTh, Prof. 0. H. SYB~JXINC), Dr. E, ASPLUXB,Dr. S, AHLXZZ~ and Dr. H. RUBN af Rantaien.
[If NRC% A. 0. and GSYLW~A.N~~N, E. A.; V&&ions in the relative abundance of the o&rbon ieti~es. J. Amer. Chem. 800. 1939 61 697, [2] M--Y, B. F. md NXBB, A. 0.; Variations in the relative 8bundance of the carbon iwtopee. Phys. Rev. 1941 lie 771. (31 RMTXAXA, K.; A note on the original lQ48 QI 189. 143 W~CKBMN, F. E., Bzxx, R. isotopic composition of terr&ri&l carbon. J. Ml. of the carbon isotopes in and YON UBISCS, If.; On the variations in the relative abuz&nee csrbonate mirier&s, 3, Ueoi. lSBf8@ 142. fb] W~GXXAX, F. E. 8nd vex Uznsca, H.; Two no* on the iwtopic co~t~t~tio~ of carbon in miner&. &so&m. et Coamochim. Acta 1951 1 1 IQ. fQ] vaN ECEERinvwtigxtion into the isotopio compoWAX?% H., ~0~4 thmc~, ff, and WICKMAN, F. R.; A pdiminary sition of carknm frcun some a&&he intruhna. Geocb, et f2ussmochim.Acte 19.52 E 207. [7f VON Foooa, J.; Wygieniwhe ~~~~~h~~~ iibw Luft, B&en und Waster. ~~un~hw~~ 1881-1882. [8] STEWART,D. W.; Isotopes. Anma Rev. of Phys, Ffiem. 19sf% 67, [S] Wsxs, J. W.; The r&t&+ of ~ho~~th~~ to reepiration. Doctors1 && Univ. of C&f,, Berkeley 1949. [ro] JFUNT,R. F. 8nd I~EVEY jr., E. S.; gibbon dating of ~~-~~~~e~~ eventa. Amer. J. Sci. 1961 %@- .26X ill] LAXDEWIWN,S. and MARVEL, A.; On the rtktive abundance of the carbon isotopes in Swedi&h alum shales. Geochim. et Cosmochim. Acte. In Preae.