Flora, Bd. 1(;6, 5. 137 - 152 (1977)

Physiological E cology of CO2 Fi.xat ion in Bromeliaceae

E. MEDTh'A, M. DF.J.OA.DO, J. H. TnOUORTON a.nd J. D. "MEDINA

Centro de Ec:ologi80~ Caracas,

Sum m ary

CrlLS!!u lllCCll1l Reid met abolism is widely distri buted &mong Bromdiaciltl~. Gas ch romatograph ic analyses of cel! sap extracted at the beginning and Lhe end of t he lig},t peri<xJ showed that mA.hue

is responsible for Ilbovu 70 % of the acidity chs.n,ges. Simultaneous concentration changes in oth er acids were detected but their significsnce is not CI68T.

Environmentsl control of CAM i ~ lIhowcd for nutrient !\upply, wmpcre.Luf<: Ilnd wiLwr supply. In ne.tural condltiolls within t ho sumo altitudin91 bcl~, ni~rogen cont-ent (and f,robably chlorophyll (lS a consequence) !;OOIDS to be positively cor relate-d with CAM activity. Temperature dependence of CO~ cxch(l,llgo ehowethat there is a temperature op1.imum near 16 DC. Wat.ersupply restriction induces CAM CO~ exchange patterns in Guzmania. fflO'Il()lJtachi(l whilo roduc{ls net OO~ guin in TillandBia ulriculaUJ. G. fflQtWJllachia is considered an inicrmodiato species, and is postulated that the bromclioid SJJfli.'i1l6 Willrockia campq8-pqrtoi nnd Nidularium i nlloC6ntii var. irm~f1tii (baood 0 ' 1 oue rMions) should b<:>have in R ~imilar way. The ecologic.:allUld "volutionllry rele"anC',.e of borde.lioe ~peeiea _ ms to be that they represent tha lin1a.ge between arid and humid habitnts in tho c1ifforontintion of the

family. Finally it is shown U".~ 0130 ral;io$ present 8. continuous spect.nJm in the family &8 a T8Sult of

.",viru,,,,,,,,,wJly cu"t.n.>U"u CAlI-I activity in Illsny Hp6cias and .Lile rliIfenmtill!.ion of typical 3C and

CAM species adapted to oxtl'Ome humid and shady or arid cnvironment~ respectively.

Bromeliaceue is a neotropic p lani fu.mily known to ocoupy IJ,. veriety of habitl~t!l.

ILS terrestrial or epiphytic fonns , fl'om humid open vegetation in high mountains to low land arid a.reas, a.nd in shady humid places in both lowltl.lld a.nd mountain forests. This diversity of hubit.llt s is reflected in mQrphologicaJ and physiological traits which aJJow a. particularly clear understa.nding of the rela.tionships between plant and envil·onment.

The fa.mily is divided in three groups ",,,hich appll.nmtly evolved in diffcrcnt en­vi.ronme nt!! and which even now present a characteristic distribution. The Pi'cairnioi­deae are highly divers ified in the Guayans. highlands and ulong the Andes ('..ordillers.; the Tillandsioideae sccm to ha.ve their cent er of dispersion in northem South America a nd in the Caribbean region, whilc the B romeliQideae have centers of dispersion of many gt:lDt:ra in northeastern Brazil (SMITH 1934). TIle evolution of the family has becn considered since the work of SCIIn'lI'E'R (1884) and TriTzE (1906), and t here have been contradictory opinions, between those which considered the evolut ion from arid areas forms penetra.ting the low light intensity and humid forest habitats (PrTTEN­

.DRWR 1948), and those who maintain that the development of at least the T illandsioi­deae, followed the reverse way (B:ENZJ:r<G and RENFROW ] 971 a" h). Recently the physiological chaJ.'a.ct.eril)tiC8 and ecological requirements, specially nut rition (BENZING

and B unT 1970) and COl!, exchange (BENZING a.nd RENFROW 19713., h ; MCWILLlA.M9

138 S. MEDINA, M . DELGADO, J . H. TkOl;iCIt'l'O,N o.nd J. D. MEDINA

1970; CoUTJ.}tHO 1963, 1969 ; NRALES 1972; NRA..LES ct. al. 1968 ; 'MEDINA 1974), of lIevera! Bromeliactae species ha.vo boon intOl:lllively studied. GIl.$ exchange experiu:acn clearly showed the existence of "wo CO2 £lXatiOIl patterns, a.) nxation of COt oruy during light periods, through the CaI"in-:Benson pIlthWBY (photosynthesis) and b) dark CO2 fixation (Crassulacean Aoid Metabolism, CAM) fl,nd photosyntbesis.

Morphological chAracteristics of Bromelia.ceae a.rc l~lso importa,ut for Lho inter­pretation of ecological behavior of the Bro7n'.liaua~. NITSK.N,BERGK (106 1) tllld Co04 'UNllO (1963, 1969) observed the relationship between suoculence, cWoroplast. distri­bution and acid meta.bolis.m, rcault8 recently confirmed hy !\U;lH.NA (1974-). CAM pla nts have bigger vacuoles and posses Muck, mostly s ucculent lea.ves, n.nd nJJ cells with CAM metabolism do have Cl hloropln.sts. The importanco of the scaleR in water upt.ake /tno nu trieut supply, stl'o ngly limiting processes in :.:eric environments, has been studied by Bt:NZlNG (1976).

Di.8Lrihutlon of OA.M within t·he family and t.he pattern of 13C discri minat.ion were 118ed as basis for lL hypot,hesis on BromtlUwtW.e evolut ion , explaining tha.L develo"pment. of xeromorphic cba ro.et.eristiCll of ancestors growing under heavy radiation IOll.d in high mountainlJ, a.nd t.he potentiality for opiphytism Q.I.'O the main traits which charac. te1'ize the evolution of the family. 1n llJ'id habitats CAM developed, and it n.ppellred iJ\dependently in several groups of the f8.Llli1y (1\b: IH NA 1974 ; MEnrN"A a nd l'aOtlOH·

TO.N 1974). It is known tha.t, at least within CrtJ.88u.laceM, photoperiodism exerts a strong

conLrol on CAM metabolism (GREGORY, SJ>l-lAR and Tul:M...u;N 1954; QUl!:LR07. 1969 ; LJ::R~ and Q UEtHOZ 1974) and more reoently it h fl.& been sbown t.ha.t e nVlromuentaJ

factors like wuter supply and temperatul'e CUD shift photosynthetic melltholi\jm trom 03 t.o CAM: and vice versa. (BENIHm et ru. 1973 ; OSl\IOl\ll et &1. 1973; K.LUO"J! 1974 ; MEDINA. and DELOA..I)O 1976). These findings tu:e of great. importance for tbe under. standing of ecological behavior of CAM plants. Dntn on t·he mcta.bolic shifts in CAM plants have been obtained mtUnly with species of t.he Cm.MUtac.eae and MesemJmjan.. lh.e:m(j.(:.eae. Among Bromeliaceae it seems to erist. Il. elonr differeutintion between the exclus ively ca type, exclusively CAM: types and some intermediate forlllS where cho.nges in pat.terns of CO~ fixo.t.ion n.ro ea..'1i ly provoq ucd. Variability in dark CO2 fh:a.tion in typical CAM species are lDlLin1y det~rmined by night temperature, while in intermediate types it seems th&t. hydrntu.re conditions are morc important. These inl.ermediate types resemble the species described by PITTKNDRlGll (1948) in Trinidad which ha.ve a. requirement for high light intensity limited only by a. higb humidity requirement.

This paper dellls with the Cat exohange charact,erist.ics of selected species of Bro­mdiac.eae in order to distinguish lhe t.hre.e a.bove mentioned types, paying special attention to the bchll.vior of an a.ppsrent.iy intornlcdilloto species reported before (M:EnINA and TROtiOllTON 1974). In addition, pa.ttern.s of u.cid changes during Lhe dny a.nd discri.m.inll.tiOIl of 13C for species belonging to t he differeots su bfamilies a.re abo included.

Physiological E cology oceo , Pixa~ion iii nrom$~ 139

M3.teriAls and l\lethods

The 81 species of Brotn81~ included in 'Iabl<ll 2 were used ill 111i_ .tudy (Il1af motllri",1 of moat Bl"37.ll ilUl species wcre kindly provided by Padre Raul.i.rlo &il.t.. Dinlctor Jan:lin Bot4.nico. Bio de Janeiro). for ~hll determination of due ratios. B:lme of them wero allt'J Ul!ed for pbysiologiUllllI$peri.

lliii-ntB. All namell u!l8C! !l()(lording to SAUTII (l~66. 1971 ). Qu exchange was 1II1!1UItlI't!d ill an open 1J)'8tt;m ulling an Infrn.rod gM an.a.Jywr as dot.tl~t.Or (AtlalyLico.l Dflv. Go.). CODdiMolU of humiwty. temperature and ligh~ Int.enAity could be controlled with water balhs and appropriate! light. rilt.eN. -Organia acids extrllote wore an.aJywd. by gas ohromatography uting tho procodure dellOribed by NuawAus and Kn<:tEt. (1971 ). - Mea&un!IIIf1nt. of due ratiOli WOI'II perfomHld through mlUll Spe<ltn).

ffil!try tL8 de!lCt'ibed fllsewhere (T.aOUOll'l'ON at. al. 19"l4). - Xitrogen content. of 1""veII WIUI delAlnnined by micro Kjllldahl and total ohlorophyll cont.ent (a + b) was mll/wuret! in IIoC(ltone extr8Cta foUowing

t.ho prooodure of B.Hl.TL"I'S:\1A (1973). Dfl.rk COl fixaLiOIl WIllIIj,JSO melWured undor :If\turnl condi~ion. both colorimatrically IUld through

mllll\UI acoumuJR.tiun dot.ormincd oD.2:ymatico.lly B-t tho bogillnill8 .md und of t be n ight (MXDJ.NA

1!l74 ).

Results and Discussion

U ark COt fixation And &ccltmu i &t.io n of organic acids

All bromeliads showing dark COg fiutioQ preseut. a. eharl:Wteristic pH fJllctuat.ion of cell sap due m n.inly to cha nges ill concentration of ma.late. Changes in malate concentra.tions normally account fo r more than 70 % of the total acidit.y varia.t;ion i n tJtcsc plo.nts (M.l!:DLNA 1974). Fig. 1 shoW'S gas chroruatogra.phic a.na.lyscs of three

CAM specics representing the different snb.faotiles of BromeUacuu!.

It c&n be seen t.hat malate (peak No.3) is responsible for t.he ma.in part ofilie flue· t,uaW on in acidity during the day.nJght. cycle. Corresponding maximum a.ccumulation

of malate in these species in thc experiment of Fig. 1 are 67,umoles/g r.w. hi D. 'ubtrosa ; 92,umoiefl/g r.w. in T . tllricul04a and 123,umoles/g r.w. in A. bromel.ifolia.

Malat.e conoentmtions vo.ry regularly, being higher A.b t he end of t he dnrk period and minimal a.t. Lhe beginning. Other acids d o not show such !I. regullU beha.vior. Cit.ric acid (peak No.5) increases duri.ng tbe night in D. 'uberosa a.nd A. bromelifolia. but. it is compa.ratively reduced during the same period in T . u' ricu/.mu. Acids which n.p penr in some of t.he gas Ohl'OIDIl.t.ogr ll.m.s, and whioh Me not rclated wit,lJ CAM metabolism are tartaric (1) (peak No.4), quinic (peak No.6) a..nd glucnron.ic (pca.k No. 7). It would be worthwhile to invesWgate t ho int.era.ntio n between OAAt and othe.r biO(lhemica1 pllthwo.ys involving organic acids in CAM phmts.

En viro nm e n ta l contro l of 0 0 2 fixa.tion in BrometiaceM

P hotosynthesis and dark CO2 llxn.tion of CM:I: Bromeliaoeae are contt'olled u nder natural conditions by nutrient supply, tBmperatnre, light &nd wa.ter supply . The epiphytic habitat oharacteristic of most Tilla·ndsioids a.nd mn..ny Bromelioids guara.ntee n. Wgh light flux , but this advantage is counterbala.nced by a minima.! eupply of nn· trienta oowing from air borne dust or organic debris from the forest canopy, Since epiphytes do not ha.ve a soil water reservoir a.vailable. they must ejt.her catch water wit.h their leaves l as in ta.nk Bromeliads (PITTENDRIGlI 1948) or ILCCUlOlllo.to it within t henl. Most e.'tia'eme epiphytes, mainly !UD.ong the Tillandsioids, possess a thick cover

140 E . MEDINA, M. DI':LCU.uO, J . H. T ltOUUHTO!f and J . D . MEOISA

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Physiological F . .I.:<llogy of CO~ Fin. Lion in Bffnltei:iaa.oe J41

Table 1. Fre.m weight/dry weightl ra~io, n itrogen and <=hJorophyll content. of loa"08 of Bromeliaccae from diffcnm~ habi tat.s growing under l1Iltu.rnl cooditions.

Sp&eiea with dark CO, fix"tion F.W·fD·W. Nitrogen Chlorophyll (mgjgd.w) (mglgd.w)

l'ilta1l<UUJ /ailciculaW 4.1 3.7 0.47 T. andrttma 4.6 3.D l.02

7'. pmmn.ril '.8 4.4 l.46

T. el<nlgaJa 6.2 ... 0.37

'J'. poly8trJChia '.7 4.5 0.4.2

T . junl:Mo 3.1 5.i UI4 T. bolbUiGna 3.7 . .- 0.8~

'1'. gardntri 7A 6.9 1.38

T. ilioCllrnata ••• 7.7 2.02

7'. ICAUdeanI:J 6.5 7.0 . .01

T. nJIIUnKlta ••• 9.2 2.1>2 2'. ~1b08o 7.' 9.' 2.4!)

T.oircinnato 9.1 10.2 l.OS

T.l6ftuiIQl.ia '.6 J2.1 /S. 12

T. j(f1%tIOItl ••• 12.6 0.99

Au/mlW 8eJ.iget'fJ. 6.1 4. 1 0.20

A. peliduliflo-ra 7.' 4.' 0.33

A . tilla~ 6.' '.0 0. 19

A. cMmtinii 7.5 .. , O.H

Spoci08 without du.rk CO~ F.W.{D.W. NiLrogen Chloropbyll finLion (mg/gd.w) (mg/gd.w)

Piuairnia jflfU:OWU 3.6 6 ' 0.33

P. proitw8t1 4.7 7.4 0.53

Broochinia micranUIlI '.0 •. , 0.4(1

Cot~(Wfia, guio.~n.ti& 2.' 10.3 0.35

TillandMG ad.,lrtJl/8illQro. '.7 4.' 0.116

T. IpicttlI»a '.1 5.5 3.67

T.jonmannii 6.2 6.6

'1'. (Bromha 6. 2 7.' 1.33

T.oompla:1Uita: 3.2 '.6 0.70

T. compoclG 3.' 13A 1.42

OalofJN ~Mno ••• 6.' 1.19

Gu..-mllniu miti8 3.' 7.0 0.52

G. aoorifolia :{ .6 ,., 1.14

Q. lriruum ' .2 11.8 2.90

Q.~ula 3.3 15.2 O.M V~",Irnd_ 5.' S .• 3.09

V. Mpituligeru 3.3 11.0 0.50

142 E. i\lJ!:OlN.A, M. D"I!:LOADO, J. H. TROUGllXO~ and J . D. MEOD>A

of water absorbing scales (BENZING 1970, 1976), which allows au efficienl.leaf water a.bsorption. These scales are rapidly sal.ura.ted, therefore, for survival of extreme xerophytio epiphytes the frequency of rainfall is more important than its absolute amount. That is the reason why bromoliads a.ro rare in cnvirorunents with strong seasonal rainfall regimo. The SILIIl.O is valid for the distribution of mo!>t succulents xerophytic plants (W.ALTER and KnEED 1970 ).

N itrogen content and da.rk CO 2 fixation

A survey of fresh wcight/dry weight ratios and nitrogen content of Bromciiaceae species representative of several habitats and growing under natural conditions is presented in Table 1. This table presents also chlorophyll content of the same leaves. I t is apparent that dark C02. fixing species, which frequently grow iu SUllUy , dry habitats, where they depend mainly on rMu and dust for nutrient supply, t end to show a. lower nitrogen oontent per dry weight as those species growing within the canopy, where they can accumulate organic debris and throughfall water, rioher in mineral nutrients. Variations observed in the. chlorophyll content eQuid be related to lower light intensities and better nitrogen supply in the habitat. Nutrient sta.tus defini· t ivelyinflucncea productivity in epiphytes, as has been shown by BENZlliG and R,EN· .PROW (1971 c) in Tillandaia ciroinna:a.

Production of organic matter in strict CA..1fi plants depends mainly on the dark CO2 fixation. Therefore a. positive rcla.tionsh.ip bCl..wcen nitrogen content of leaves a.nd tota.l da.rk COa fixation was expected. Fig. 2 shows this relationship ill CAM Bro· meliaceae growing at different alt itudes in t ropical mountains. I t appears that within

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l'hy~iological Euology of CO~ Eixa.tion in Brom~~ 143

each habitat, there is a tendency for higher dSI·k CO~ ultaLion in plants wjth higher nitrogen content, although differences bet\vcen hll.bitats Ilrc also pll.rlill.lJy determined by night temperatures.

Photosynthesis a.nd tho temperll.tur.e dependence of dark CO 2 fixation

.Net increase of malate content in cm plants during the night is tbe result of synthesis clue to the PEP-carboxylase-malate dehydrogenase system and the decar­boxylation mediated either by NADp malic: e.ll:l.yme or by PEP-Carboxykinase (D:rrr­RIOH et a1. 197:3). Temperature dependence of this process has been accurately in· vestigated by BnA.l<"DON (1967), who found a.n optimum near 15°C for in vitl'O dark CO2 fuation in Bryophyllum lubiflorum. Measurements of totaJ COli exchange during day-night cycles at different temperatures in Tillandsia recurvata show (Fig. 3) the rela.tionships between dark CO2 fh:o.tion and photosynthetic CO2 fixation. Temperatu­res above and below 16.4 °0 reduce net gain duting the period. It also soems that a lower dark CO2 fixation is followed by (L higher uptako of ex~ernal. CO2 during tho day. This nea.rly inverse relationshjp botwoen night and day CO2-uptake is presented in E'ig. 4. The reason for this behavior is that in CAM pln.nts photosynthesis has two sources of CO:: (KLUGE 1968): a.) CO! coming from decarboxylation of malate acen-

Tilla!ldsio ,~Curval(}

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NIIIIH T£J.f> 2 •. C "C

IlIG!1f Tt"IP. 1.1"{

144 E. MEDlNA, M. DELGADO, J. H. '!'ROtlGHTON" Ilnd J. D. "MEDIN",

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Fig. 5

Phyaio!ogic:al Ecology of CO., Fixation in IJrom~i<ICf!(Ul. 145

mnla.ted in lohe vacuole during t he previou s night. lind b) external COli entering the plant through Lhe stomata. Active night CO! fixat.ion mea.ns that duriug next. day chloroplast. environment will be sa.tura.ted wiLh CO:!;. si.omat.a will remain closed and net CO! uptake from outside will be observed only when e ndogenous COt has bee.n co nsumed and stomata. open a.ga.in .

Thi.s situation dir[icult9 the in terpreta.tion of photosynthosis lighl, cUI·ves in eMf pla.nts. F ig. 5 shows Lypica.llight curves or photosynthesis in B romelitwwe. T illandsia spioulosa, & Os bromeJiad and '1'. re(;urval(" a. CAM bromcliad, behave differently regarditlg the raLes of upt.a.ke ofexogenous COs. It Ilppetl.rll t hfi L the CAM bromeliad is sa.turated, at very low light intensities a:ld CO! exchange is minimal in comparison with ra.te~ observed in 1 '. spiculoso.. But it is clear Lho.t the neL CO!! exchange is depen­dent on light in!.ensit ies in the sam e way in both speoies. A~ low light intensity during th o day period, ~l' . ,.ecurvala. looses COz coming from the d eeB.l·boxylatiOIl of mala t e

alld in darkness, CO2 ouLput is sc\'eral times higher tha.n in T _ spic-ulosa. Measurem.enLs of t.emperature dependence of total da.rk CO2 fixa.t.ion in species

of BrOlfdiaceae g rowinit at different altit.udes do not show marked varia-Lions in tho optim um temperatm·c. Fig. 6 presc nLs thew. temperature curves of T . T~curva'a and T. ut ,.iculata from habil,aLs at 1600 m (H." u.nd T. Tcourva'a from ha.bita.ts at sea. level. Optimum t emperature for dark CO2 fi.xa.tion seems to be loca.ted around 15 °C. Appa.rently there should exist II. tcmpera.ture·compensating mechanffim which results in similar temperature optimum for pla.nts from different aJtitudinnl !Jolts. In !lny CI\S!l, t.cmpera.~l.I re ada.pta.tion of CAM deSeL"Veli a morc detailed a.na.lysis.

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~' ig. 6

146

Da.rk CO 2 fixa.tion and water content of the leaves

Water supply hM been a.ssooiated with CAM in two ways. Firstly the rhythm of dark CO2 fixation is correlated with stomata. opening at night (NISHIDA 1963) probably due to increased leaf watcl" potent.ial Kr,uoE Mel mellER (1967) clearly demonstrated that the rhythm does not depend on stomata. opening, showing in Bryollhyllum daigremontianum. tJlat leaves without epidermis present the same CO2 fixation pattern. There exists then, an internal control of dark COt fh:ation follO'\\"ing

aD endogenous rhythm. l 'his fact has been recently documented and ana.lyzed (QUEI­

ROI'. 1969, 1974; BRULFERT et al. 1975).

Secondly, dehydrat.ion seems to illcre.ase the ~ctivity of the PEP-carbox:ylasc­malate dehydrogenase system resulting in ~ more pl'onollnced CAM pattern. I n­creased dark CO2 fixation correlated with L.issue dehydra.Lion has been shown in

Crassu~ (MEullTA. a.nd DELGADO 197 6) and also in a bromeliad, '1'. UJnCQlde.s

(KLUGX et aL 1974). NeverLhdcss dal'k CO~ fixation is reduced if plants are sub­mitted to severe water strC>JS. KAUSCH (1965) in Opu,n'ia puberula and SZA.REK and Tow (1974, 1975) in O. basilaris were able to show that after several weeks of no water supply through the roots, no gas exchange could be detected , even though daily changes in tissue malate content could be demonstrated.

In this respect the induction of CAllI behavior in plants norma.lly performing as 0 3 is ecologically relevant. Guzmania monostachia JHI.s been reported as a p lant having this type of LransienL adaptability (M.I!lDIN.A. and TROUOl:{TON 1974). The CO2 exchange

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Physiologies.! Ecology of CO, 'Fixa.tion iD. BN»nelia~

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147

patteI'll ullder oonditions of p rogre3!'1 ivc wuter stress is shown in Fig. 7. I nside Lhe photosynthesis ohamber, at M % relative humidity dudllg Lhe light period and an a.ir fl ux of 500 TU I/min, t he planL looses wat.er ra.pidly a.nd the co nsequence is a. I'educ­tion of C0 1 fixat.ion during the day and an increa.se during the n.ight.. If after 5 days in the chaw bel' the plant is rewatered for 10 minutes (with a complete recovery of lost waLer) t.be CO2 exchange pattern goes bllck Lo ihe initial condit.ion: uet CO2 gain

during the day a.nd CO2 1038 duriug the night. Fig. 8 shows the inverse relationship between net dark CO2 gai.n liud the reduct:ion in fresh weight.. The same treatment o n T . utricukUa shows only reduotion in net COl! fixa.tion during t.he night.

6 18 0 dis t dhution wit.hin the family a nd its evolutiona ry significance

Discrimination of bUG showed in mass s'pect.rometrio analysis of organic mRtter in higher pla.nts hILS hoen used Q.S an indication of the primary ca.rboxylat.ion iltep i ll

CO! fh:(I"tion (1'ROUGBTON et a.l. 1974). <; a.nd G" pla.nts can bo neatly differentiated by this teohnique because t.hey show a discontinuous spcctrulIl of 61:3C values (SAllTIT and E pSTEIN 1971 j SMITU and BROWN 1973).

Analyses in sorveraJ species of bromeliad showed a clear distinction between CAlL a.nd ~ bromeliad species (M.EDINA a.nd 'l'ROUGBTON 1974 ), this WaI! interpreted as an indicat.ion of PEP.cn.rboxyiase being -the ma.in enzyme media.ti ng entrance of CO~ a.nd ol'ga.nic ma.tter a.ccumula.tiOIl in CAM bromeliads, while it is R uDP-oarbo­xyla3e in Ca.

CAM plallt6 do not ha.vc a. struotured compart.mentation of ca.rOOT.'ylation and docarboxylation st.eps in malate synthesis a.nd photosynthet.ic utilizat ion of Utis acid . Therefore t he explans.tion for CAM plants showing high dtSC ratios s.houid be t ha.t the deca.rboxylation reaction wit.hin tho cytopia.sm is intensive enough to ma.int.a.in

148 E. MIDL ...... It'. DnoAno. J. H..1'aoCOIn'O~ and J. D.lI.ItDcu.

Spec,- "'""" ~.,.

lko«MniD lain Vc:nuuela -27.:1

lJt.eqa 'wbfnMG BlaxU - 12 .• ErlCltultri"", IIotA __

Dta&.il - 1%.4

I'tI('Olm.o prvinOlG ven"'"uel .. - ::6.0 P. /10m".. BrarJI -27.9

PI/YO II/pc""" -! . ... I', kl"ltII'O"ilIn(f Ch.Ju _ :to.9 P. cJ,ikr14Y Chilo - 17.0 P. coll1llpirkJ Chila _ 11\.4

P . Ikrt4i{loNl SouLlI A.IIM!ril!. -20Ao

I'. did.~u South MIM!riea _2t.7

P·/crrvri- PON -24.8

P.p- V_ucla - !!Ui P pofwl_ SoIith Amenna - fU P. rolrHPtdii South Amerie& - :2.7 P. tIIltWIfa Ch'" -23.:

c~,.",- V_. - H.' C. _.lIjlonJ Brall - U.7 G.-.. lG",r . +Ia V"""",Jo -fl.? O.",~MIo Vecea.uela -21.' 'l'tUc.rvhto OCIPltploKalO V.lleltuela - 2U T JJdf'"UO V_UteI. - '5.3

'1'. adpru.t/llJro VUlle¥~I. - 26.:1 r .a_p' Vena_I. -!8.3 T. aNireoAO VODOllleJ" - 13.3 T . Pf'Uujei Srar.!! - 14.,3 7'. boIM.n(IIIG Vell~uC! l. l It! T . b"lbofa Brlll'.l1 - lO.a: T. eimnmUCI Venezuela - 1!t.7

T. et1IIIpackI VcuwnulJ. -2:5.6 T. /endl.vi Veue&U(lla -24.8

T .1IfII'd-' V_Ut'la - 13,0

'f'. l--''' Vf!net:\lela _ 1110

7',101_ Bran) - 16.: T. ,..CII"",I(I Vell~uel. - 15.3

'1' •• ptCtJ.oMJ VeuUtuela -U.o T . _rep' po Bruil _ I!..

T.~ "...u -17.3 '1'. btli/olra V..-..Io _15.!

'I' . ......"w.. Ven.-1It'1a - 12.7 7'. III~a Ven8U(!1a - 13.7

l',.....plQ4~ V.uCIIlld .... -!s.e I' . ".-ru B""" - '7.9 V.~M 8""" -~.,

Physiological Ecology of CO, FiXClt.ion in .Brornai_e 1<9

Table 2. (Cont.) ~I'C vu.lu6fI of BTomtllauae (leaves): Bromeli.oidwe

Species Origin 6l'C G/ou

..1cu"llio.tt.lchYI"robilOilell Brn%il - 14.11

A echmw tiUan(Uiodu ,Tcnczuela - 15.~

.4.. bromali/olw V8lle:r.uela - 13.6

A. b!andlUiana BTIlZii ~ 13.U

A.lingulaM Braz.il - 16.7

.'I. peelinala. BrnZJI - Hi.7

A. gamoupcJIJ I3mzil - 15.'1.

ATa4lOCOCCIl" mWrlJlll.hWl BI'8z.il - 16.7

BillO~rgia portcafl(l Bl'I}.;I;Li - 12.0

B. aflHl6na I3m-r;i1 - HUI B. pJlTamidal16 Brazil - 15.6

nromelw humil" Vellczuchl. - 14.1

Ctmi"INlm U"dtllii var. fOleum Bruil - 18.3

C. trionguw"" Bm:til - 16.3

OryplimJIIIUI lip. Braul -17.8

OryplmUhuI bf'Omeliotdu Bm:til - 16.2 HOMnbergia ulrie-ul4)&(f Brazil -12.'1 H. cf. lUlomli. Brazil _ 12.1

H. N lzman"ii Bra7.i1 _ 15.;

H. di.rjUfleta Bruz.il - 17.1

H. brachyuplwlL< BrllZiI -16.6

.Noogla:ioIJla 'lJl'lriegaw Brn7.J1 - 13.4

Nw~w. cruema Brazil - 14.0 N.wr&ac- Bra."'1 lli.S

N. CQIu:entrtM Bra.,;;1 - 15.9

N;d~ri.llm #MrCllllOl'Uf'ji Bmr.il -16.3 N. illtWll4:lnlii ,'ar. mno.·enlii Bmzil - 2'4.0

OrUwphytum 'a%iaIla Bru.il - [6.4

O./oliolum BnWI - 17.2

Porl.w petropoli4lna Brn.:ti.l - 13.6 QI'uJWlliu mormorata BrlU:iI - 14.2

Q. 'l"r.ltnduma Brazil -1 3.7

SIrepUXX'/II:JJ po8ppigii I3razil _ 14.0

S./UwibUfldw Bra:.iI - lUi

Tl'itlrockw camprH·portci BmGil - 23.1

lV. #UptlroQ- Brazil - 16.4

RuDP-carboxylasc under a. high CO2 concel~tnl.t.ion and to reduce eOi diffusion from t.he environment .

.Environmental re~ula.tion of CAM, a.nd tJle existence of intermediate specics such as Guzmania. lIw'IIoslacli.ia , known as a potentia.l GAM plant with low 151:1() ratio, would allow tb e pl·cd.iction thnt the spectrum of 01:1.0 values within the whole family should be a continuous one. Ana.lysis of leaves of 87 species belonging to the throe subfamilies a.nd coveling tho wh.ole range of ha.bita.ts oc:cupi6d by the family, gave the results presented in Table2. The spectrum of dllO values is shown in Fig. 9. There is a. con tin­~ .FlO,., 8d. lOll

150 E.l\1.&DOfA.. M . DY-WAno, J . H . Taouotrl'O:IO" and J . D . MEDINA

BROMH IIlCEAE 13 N~87

" " • 0 ~ 9

~ a o '

l : , . , , o • ,

" " "

Fig. 1.1

UOll5 variation [l'om - 12 to - 28.6. Another tendency conld ue obscl'ved among th e­subfamilies. I t seems that tho Pi.tcairnioideae have lower diSC ratios . while most BronulioidtM examined pres~nt higher ratios. I n TiUand8ioidoo.e the dirferentialion of C;, CAM a.nd intermedia.t.e t.ypes is reflected by 61SC ratios covering Lhc whol6 range. If t hese tendeucies reflect the rea.l situH.Lion. it provides support to Lhe hy po­t hesis on Bromclia.ceac evolution p roposed eal'lier by MJWT.NA (1 974).

Within t·he Pi'cairnioideiu, tbo phyiogenetically oldest subramily. the capa.bility of CAM development 1S present ns shown by genera. Djckya. and ElIGholirion. In a.ddi­

tion , the varia.tion within the genus 1?1tya is Ii clear indication of the existence of environmentally regulated CA~f (noti ce the range of P. c1~ilensl~8 from - 17.9 to - 21.2) . Many Pilcairnioideae ill t.he Andes ha.ve been able La invade relat.h·ely xeric babitats. On tbe other hand, in the Bromelioidcac studied, CAM metabolism seems to predominate, but some reduction of its import.a.nce for ca.rbon balance in somo species mn.y be noticed. The 4 species of Oryptu11thu8 (1\ genml wit.h several species growing on t im ground LD h umid forests) studied, show 013C \'alues, closer to typi cal C3 • whil6 lI'illrockia c.a:mpoo.port.oi and Nid1tlarium imwce7IJii have t.ypical ~ 6130 va.l ues. IT we assume that Bromelioidea.e evo lved in xerophytic environments, one should expeot tha.t a. subsoquent invuion of shady, humid habitats lUay result in 8. pro· grossive 108s of xerophytio eha.racters, im:ludillg CAM metabolism. We p rediot that gas exchange pa.tterns in the Ift!;t two species wo uld be. similar to t hat, reported here foJ' Ou:;ma1tia tnO,w8Ulchia.

1tefcrences

BGNOKU., M., RO IJ'KA!"T. l ., VOO1I.:S, H . M., IWd DLAOlt, C. O. Jr. : 130 / 110 ra.tio ohauge.e in ort\.96uIJlCe(Ul Jl.(Iid metaboliam plant.s. Plant. Phyaiol. 52, -'l27-4S0 (1973j.

BCN"~O, D. H .: F oliar pormoabilu.y and ilie abaorptiOD of mineral -.ud orglUlic Nil.rog<Il\ by cerl..ul tank DromeliadlJ. &t. Go.z.. I3l. 23 - 31 (H)70).

I?hYlliotogioaJ Ecology of COli F'ixlllion in BromeliCJ~ 151

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KT.OOe:, M. l Ontel'lluehungen ilber den Gaswll(lh llCl lion Bryophyl!um willirell.d dOl' Lich t.ptlriode. ll. BeziebungCII :.:wisohan dom Mallttse],alb dea BlattgewebM uml del' COt-Aufnahme. Plante..

(Bor!.) 80, 359-377 (1968).

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".

152 E. J\:I);nfNA, M. DEJ,.GAUO, J. H. TRotl'oIITo!l" and J. D. MEDI~A, Physiologionl Ecology

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Received September 10, 1976.

Aut hon!' acldre~s : Dr. E XNE8TO i\IEDINA, Centro de E cologla IVIC, Apdo. 1827. Caracaa, L ie. Milena.Delgsdo, Fac. Farmaoia, UCV; D r. J OHN TROUGH'l'ON", Dep~. Sci. Ind. Res ., New Zealand; Dr . .JosE D. ?lllmnu., CentT<) do Quimicu, IVIC .