Seasonal Changes in the Phloem of Ephedra californica Wats.
Author(s): Frank J. Alfieri and Pauline M. Mottola
Source: Botanical Gazette, Vol. 144, No. 2 (Jun., 1983), pp. 240-246
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2474649 .
Accessed: 03/11/2014 07:19
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
.
The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to
Botanical Gazette.
http://www.jstor.org
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
BOT. GAz. 144(2):240-246. 1983.
(C 1983 by The Universityof Chicago. All rightsreserved.
0006-8071/83/4402-0018$02
.00
SEASONAL CHANGES IN THE PHLOEM OF EPHEDRA CALIFORNICA WATS.
FRANK J. ALFIERI AND PAULINE M. MOTTOLA
Departmentof Biology,CaliforniaState University,
Long Beach, California90840
Mature sieve cells were presentyear-roundin the secondary phloem of Ephedra californica Wats.
In a given year's growthincrement,all but the last-formedsieve cells (three to four layers) died the
same season in which they were produced. The last-formedsieve cells overwinteredand remained
functionalthroughoutthe firstpart of the new growingseason. Cambial expansion and differentiation
of xylem commenced simultaneouslyin early February.Phloem differentiation
followed xylem differentiationby ca. 3-4 wk. Cessation of functionbegan in mid-Marchwith formationof definitivecallose
on the overwinteringsieve cells and continuedto the sieve cells of the currentseason's early phloem.
ceased simultaneouslyin late May. Xylem and
Cambial activityand xylemand phloem differentiation
phloemdifferentiation
resumedin late September,apparentlyin responseto unseasonal rains in summer
and fall, and ended in late December, when all but the last-formedsieve cells that overwinteredhad
become nonfunctional.
Introduction
Material and methods
MembersoftheGnetalesexhibitanatomicalfeaturesof both angiospermsand gymnosperms
and
thushave been consideredan evolutionary
linkbetweenthetwo(BAILEY 1949; BENSON 1957; SPORNE
1965). Withquestionsof theirphylogenetic
placementin mind,numerousstudieson phloemstructurein theGnetaleshave beenundertaken:Gnetum
(THOMPSON1919; ABBE and CRAFTS 1939; BEHNKE
and PALIWAL 1973), Ephedra (THOMPSON 1912;
PEARSON 1929; ALOSI and ALFIERI 1972; BEHNKE
and PALIWAL 1973), and Welwitschia(EVERT et
al. 1973).
Studies have been undertakento elucidatethe
seasonal changesin the phloemformany species
of angiospermsand gymnosperms
but not forany
memberof the Gnetales. In addition,while gymnosperms from northern temperate regions have
been studied, except forthe seasonal study ofJuniperuscalifornica(KEMP and ALFIERI 1974), there
are no comparabledata on gymnosperms
froma
xerophyticenvironment.
Ephedra californica Wats.,a profuselybranched
shrub with xeromorphicfeatures,occurs in the deserts of Southern California and has characteristics
peculiar both to angiosperms (e.g., secondary xy-
lem withvessels)and gymnosperms
(e.g., secondary phloem with sieve cells).
The anatomical dissimilarities between the
phloem ofEphedra and that of othergymnosperms,
in conjunction with the arid habitat of Ephedra,
inspiredthedecisionto examinetheseasonalgrowth
of E. californica with emphasis on the phloem.
Manuscript received August 1982; revised manuscriptreceived January 1983.
Address for correspondenceand reprints:FRANK J. ALFIERI, Department of Biology, California State University,
Long Beach, California 90840.
Samples were collectednear Joshua Tree National Monument,Riverside County,California.
At least threeplantswere sampled weeklyduring
springand summerand bimonthlyduringthe fall
and winter,fromMarch 1969 to February1970.
Samples fromlarge, basal brancheswere fixedin
FAA solution(SASS 1958)and aspiratedin thelaboratory.The tissueswereembeddedbythecelloidin
method(SASS 1958).
Serialcrossand radial sectionsofeach collection
werecut at ca. 16 plmon a slidingmicrotomeand
thentied onto slides withno. 60 thread.The celloidin was removedwith ethylether.The tissues
weregraduallyhydratedand stainedwiththeferric
chloride,tannicacid, and lacmoidstain(CHEADLE,
GIFFORD, and ESAU 1953). Callose and dignified
cellwalls stainblue withthisstainingcombination.
Results
GENERAL DESCRIPTION OF THE BARK
The peridermstypicallyare laid
downin concaveplates,withtheconcavitiesfacing
outward,impartinga scalloped appearanceto the
outerbark,as seen in crosssection(fig.1). A peridermis formedeach season, and several seasons'
peridermsand the phloemtissueisolatedby them
may build up and be retainedforsome time(fig.
1). Each season a new peridermoriginatesin nonconductingphloem,just internalto thefiber-sclereids produced in the nonconductingphloem the
previousseason (figs.2, 3). This occursduringthe
latterhalfof March by the initiationof a layerof
phellogenfroma uniseriatelayer of phloem parenchymacells that expand and begin to divide
(fig.3). By mid-Aprilthenew phellogenhas begun
to produceseverallayersof corkcells (phellem)to
itsoutsideand severallayersofphellodermcellsto
its inside (fig.4). As the cork cells mature,they
PERIDERM.
240
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
FPP
t'~~~~~~~~~~~~~mW
4
P
4~~
A
~
~
NP~r
FIGS. 1-4.-Ephedra californica. Fig. 1, Cross section throughstem, showing scalloped appearance of the outer bark or
rhytidome(Rh). Collected January3, 1970. x 67. Fig. 2, Radial section showing periderm(Per) and nonconductingphloem
(NCP) with fusiformphloem parenchyma cell (FPP) containinglipoidal substances. Collected February 28, 1970. X 350.
Fig. 3, Cross section throughstem during surge of cambial activity.Site of originof most recentphellogen (Pg). Collected
March 29, 1969. x 215. Fig. 4, Cross section throughstem showing conditionof phloem in late spring. Callose (unlabeled
arrows) has built up in sieve cells of early phloem. New periderm(NPer) formationis evident. Collected May 3, 1969. X
380. X = xylem,V = vessel, CZ = cambial zone, CP = conductingphloem, SRC = sclerifiedray cell, FS = fiber-sclereid,
MR = multiseriateray.
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
242
BOTANICAL GAZETTE
remainthinwalled,and bymid-May,deeplystaining resinousmaterialbeginsto infiltrate
theirlumina. This appears to be theonlytypeof corkcell
producedin Ephedra californica.The phelloderm
cellsare at firstthinwalled (fig.4), but by theend
ofMay theybeginto sclerify.
Corkand phelloderm
productionand differentiation
appear to be continuousthroughout
the growingseason.
NONCONDUCTING PHLOEM.
The nonconductingphloemliesjust internalto thelast-formed
periderm (figs. 2, 5). With the formationof a new
phellogeneach yeardeep fromwithinthe nonconducting phloem, this region is preventedfrom
buildingup fromseason to season, and, consequently,it remainsa relativelynarrowarea. Because ofcircumferential
expansionassociatedwith
each season's growthincrement,increasingpressure is applied to the cells of the nonconducting
phloemso that the dead sieve cells and theirassociated albuminous cells collapse and become
crushed,givingan overallwavyappearanceto this
area (fig.5). Phloem parenchymacells are either
fusiform
or two-celledstrands.These phloemparenchyma
cells,whichdo notdie at thistime,begin
to expand bothtangentially
and radiallyand may
accumulateamber-colored
lipoidalsubstances(figs.
2, 5). Some parenchymacells in the two-celled
strandsmay become sclerified,while othersmay
contributeto new phellogenformation.The fusiformphloemparenchymacells in thenonconductingphloemmaybe transformed
intofiber-sclereids
(figs.3, 5). These cells graduallybuild up thick
secondarycellwalls,which,withthelacmoidstain,
appear lightgrayto grayish-purple
earlyin their
In later stages of differentiation,
differentiation.
these cell walls stain increasinglymore blue, apparentlyin directproportion
to theirlignincontent.
The wallsofmaturefiber-sclereids
stainthedeepest
blue. The differentiating
fiber-sclereids
are
typically
locatedjust internalto the innermost,or mostrecentlyformed,phelloderm(figs.3, 5). As withperidermformation,fiber-sclereid
formationdoes not
appear to coincidewithany othergrowthactivity.
The multiseriaterays generallydo not become
distortedin the nonconducting
phloembut retain
theirstraightand orderlyappearance (figs.1, 3).
Some ray cells in thisarea may become sclerified
(fig.3).
CONDUCTING PHLOEM.
The axial systemis
composed of sieve cells, albuminous cells, and
phloemparenchymacells. Sclerenchymacells are
notpresentin theconductingphloem.In crosssection,the cells of the axial systemare laid down in
an orderlyfashion,producingneatlyalignedradial
filesthatbecomeonlyslightlydistortedin thenonconductingphloem(figs.5-8).
The sieve elementsgenerallyare rectangularin
crosssectionand are recognizedby theirrelatively
clearappearanceand primarycellwalls, whichare
slightly
thickerthanthoseoftheotherphloemcells
(figs.5-7). Their tangentialand longitudinaldimensionsare 15 [m and 400 [Lm,respectively.
In
radial section,the end walls of the sieve elements
are extremely
tapered,and thesieve areas are uniformly
distributed
alongthelongitudinalwalls, althoughmorecloselyspaced on the end walls. The
amountof callose on the sieve areas is directlyrelated to thelatenessof the season. Degeneratenucleiofthepycnotictype,stainingdeep purple,were
commonin maturesieve elements.Some sieve elements originatefrom phloem mothercells that
undergotransversedivisions;consequently,some
sieve elementsare onlyhalfthe length(about 220
[m) of others.
The albuminouscells have densercytoplasmic
contentsthanthesievecellsand staina lightpurple
with the lacmoid combinationstain. They retain
nucleiofnormalappearanceand have lateralconnectionswith the sieve areas of contiguoussieve
cells.In crosssection,thesegenerallysquarishcells
can be seen as radial filesdistributedat irregular
intervalsamong the radial filesof sieve elements
(fig.6). Axial albuminouscells are generallyonehalfthelength(about 220 pm) of a sieve cell since
theymost oftenresultfroma transversedivision
ofa fusiform
phloemmothercell. Theyare usually
arrangedone or twocellshighand do notgenerally
existin longitudinalstrands.
Phloemparenchymacells are eitherfusiform
or,
as a resultoftransversedivisionsofphloemmother
cells,occuras two-celled
strands.Theyretaindarkly
stainingcytoplasmiccontents.As seenin crosssection,thesecells seemto formtangentialbands (fig.
8) thatalternatewitheveryone or two tangential
layersof sieve elements.The parenchymabands
maybe interrupted
at places, and theparenchyma
cells then may appear to be scattered.The parenchyma
cellsalso appear rectangular
in crosssection but are much narrowerradiallythan sieve
elementsand albuminouscells.
The multiseriate
raysystemhas bothuprightand
procumbentparenchymacells thatare oftenirregular in shape, and in thewiderraysthesecells are
borderedby shortfusiform
or elongatedcells. No
albuminouscells were observedin the rays.
VASCULAR CAMBIUM. The vascular cambium
is nonstoriedand consistsof ray initials,fusiform
initials,and theirrecentderivatives.The cambial
zone varies seasonallyfromabout fourcells thick
duringthe winter(fig.5) to about eightcellsthick
duringits peak activity(fig. 8). The cells of the
cambial zone are distinguishedfromthe mature
phloemcells by theirdense,granularcontentsand
theirverythinwalls. The radial walls ofthecambial cellsare invariably
thickerthantangential
walls
(figs.5-8). In crosssection,thecambialcellsappear
flattened
radialfiles.
radiallyand alignedin orderly,
Theirradialdiameterrangesfrom2.5 to 5 [m, and
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
ill~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
_ s ^ SiX _ S S_r t0 S = B; L; ...E ...
_~~~~
_
A
*t~ow
Fig8
Prtin f sem
,,1
t pakof
ambal
ctvit
ColetedMarh
2,
969 x
50
d
iffreniatngxylm,
ZE
FIGS. 5-8. Cross sectionsthroughstemofEphedra calioornica. Fig. 5, WintercPn
on of mostrecentphloem increment
and portion of periderm(Per). Collected January 3, 1970. x 473. Fig. 6, New, differentiating
xylem (Xd) in firsthalf of
February.Collected February 14, 1970. x 473. Fig. 7, New differentiating
phloem (Pd). Collected March 3, 1969. x 825.
Fig. 8, Portion of stem at peak of cambial activity.Collected March 29, 1969. x 350. Xd = differentiating
xylem, CZ =
cambial zone. OSC = overwinteringsieve cells CP = conductingphloem, NCP = nonconducrting
phloem, Pd = differ-
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
244
BOTANICAL GAZETTE
winteredhave been crushedfromcircumferential
expansion. The earliest-formed
sieve cells of the
currentseason'sincrement
have beguncessationof
function
withtheaccumulationofdefinitive
callose
on theirsieveareas. These sievecellsthenlose their
contentsand collapse(fig.9). Cessationoffunction
SEASONAL
CYCLE OF PHLOEM DEVELOPMENT
continuesduringJune,and by mid-July,
most of
Duringthe winter(late Decemberto earlyFebthe currentseason's early phloem sieve cells are
ruary),cells of thecambial zone are dormant,and
dead and collapsed. Concomitantly,
livingparenthe cambial zone is about fourcell layers thick.
chymacells in thisregionexpand (fig.10).
Approximately
threeto fourlayersof cells immeMost ofthecambiumremainsin a dormantcondiatelyoutsidethecambialzone are maturephloem ditionuntilthe followingFebruary.At the end of
cells,includingthelast sieveelementsto be formed September,however,xylemand phloemdifferenbeforethecambiumbecamedormant(fig.5).These
tiationis reinitiated
in someregions(fig.11). These
constitute
themature,overwintering
sievecellsthat active regionsof the cambiumcontinueslow proremainfunctionalthroughoutthe firstpart of the
ductionand differentiation
of xylemand phloem
new growingseason.
cellsthroughOctober,November,and intothelatEarly in February the cambial cells increase terhalfof December(figs.12, 13). By late December,differentiation
slightlyin radial diameterto 3.5-6.0 tAm.This is
seems to have ceased, and the
cambial zone appears to be dormantonce again.
followed,on thexylemside only,by cambial cells
All sieve cells are dead except the threeto four
undergoingdivisionand radial expansionup to 10
twicetheiroriginaldimension(fig.6).
layersthatwilloverwinter
immediately
outsidethe
VAm-almost
These expandingcambial derivativesare differ- dormantcambial zone (fig.5).
entiatingxylemelements.None of the cells of the
cambialzone appears to changetangentialdimenDiscussion
sions at thistime. The radial cell walls appear to
It was generallybelieved that eitherxylemdifthinout slightly,
whilethetangentialwalls remain
orthat
ferentiation
precedesphloemdifferentiation
verythin.By theend ofFebruary,all cambialcells
in mostgymnosperm
thetwo beginsimultaneously
have expanded,and periclinaldivisionsoccur on
species(BANNAN 1955; GRILLOs and SMITH 1959).
boththexylemand phloemsides. By earlyMarch
It has since been demonstratedthat, in selected
new phloemdifferentiation
is apparentas theouter
conifers(ALFIERI and EVERT 1968, 1973)and diftwoto threelayersofundifferentiated
cambialcells
fuse-porous angiosperms (EVERT 1962, 1963;
on the phloemside expand radiallyand begin to
differentiate
(fig.7). During thissurgeof activity TUCKER 1968; TUCKER and EVERT 1969), phloem
differentiation
precedesxylemdifferentiation
or,as
in March, the cambial zone increasesto seven or
has beenshownin ring-porous
angiosperms,
phloem
eightcell layerswide-the greatestcambial width
and xylem differentiation
are initiatedsimultaof the season (fig. 8). Followingthis growth,all
neouslyin spring(ANDERSON and EVERT 1965;
cambialcellsexpandradiallyup to 11.5 VAm.
Their
DERR and EVERT 1967).
tangentialdiameterrangesfrom15 to 21 VAm,
and
Our investigationshows that,in Ephedra calithelongitudinaldimensionrangesfrom300 to 305
precedesphloemdifBy theend ofMarch, two to threetangential, fornica,xylemdifferentiation
VAm.
by3-4 wk. Thus, comparedwithother
uniseriatebands of parenchymahave been formed ferentiation
ring-porous
in the new season's increment(fig. 8). Then the
species,the seasonal growthcyclefor
E. californica, a ring-porous
gymnosperm,
appears
sievecellsthatoverwintered
fromthepreviousseato be unique in havingxylemdifferentiation
son's incrementbegin cessationof functionwith
precede phloemdifferentiation.
theaccumulationofdefinitive
calloseon theirsieve
Xylemdifferentiation
beginsin earlyFebruary.
areas.
Phloemdifferentiation
beginsabout 1 mo laterin
By the firstpart of May, the cambial zone has
March. By the end of March, almost the entire
decreasedto fivecelllayerswide,and thecellshave
phloemincrement
is formedin onlya 2-wkperiod.
once again becomeflattenedradiallyand acquired
The amount of phloem produced each season is
thickenedradial walls. The radial diameterof the
about two or threecell layersless thantheamount
cambialcellsnow measures3.5 tAm.Whilephloem
of xylemproduced. Xylem and phloemdifferenand xylemdifferentiation
continues,productionof
tiationcease simultaneouslyby the end of May.
thesetissuesappearsto have ceased (fig.4). By the
Since theperiodof growthis only3 mo in thefirst
end of May, the cambial zone once again appears
dormant(fig.9). It is now threeto fourcell layers partof the year,thisseems a fairlysignificant
lag
forphloemdifferentiation.
wide, and radial and tangentialcell diametersare
In additionto the normalgrowingseason at the
thesame as theywereduringwinter
approximately
beginningoftheyear,a smallamountofxylemand
dormancy(figs.5, 9). The sieve cells that over-
theirtangentialdiameter,from14 to 20 VAm.
In
radialsection,fusiform
initialshave a longitudinal
dimensionrangingfrom230 to 300 VAm.
Ray initials
are slightlyelongatedto nearlysquarish in cross
section.
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
I~~~~~~~~~~~~I
diffretiatigxye,Pd
difretainphoem
PP _ phomprecya
FIGS. 9-13.-Cross sections throughstem of Ephedra cai~fornica. Fig. 9, Cambium approaching dormant condition at
end of May. All but the most recentlyformedsieve cells are collapsing (CSC). Collected May 31, 1969. X 882. Fig. 10,
Dormant cambium at end of July. Collected July 26, 1969. x 570. Fig. 11, Cambial reactivation (expansion) at end of
September.Collected September27, 1969. x 882. Fig. 12, Newly produced xylemand phloem in October. Collected October
11, 1969. X 813. Fig. 13, Cambium approaching second dormant condition in early December. Collected December 6,
1969. X 951. X = xylem, CZ = cambial zone, CP = conducting phloem, NCP = nonconducting phloem, Xd =
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
246
BOTANICAL
occurredfromlate Septemphloemdifferentiation
however,was
berto earlyDecember.This activity,
areas of the cambium.
observedonlyin restricted
It neverinvolvedthe entirecambium.
rangesare exAt thecollectionsite,temperature
treme.FromJulyto earlyOctober,maximumtemperaturesdo notusuallydropbelow 100 F. Winter
temperaturesare low, and snowfallsare not unusual. Precipitationis sporadic,with mostof the
rainfalloccurringin Februaryand March. A 3-mo
growingseason would not be unusual fora plant
such as E. californica,whichbeginsto experience
and lack ofmoistureas earlyas
hightemperatures
late May. Climatologicaldata providedby theEn(U. S.
ScienceServicesAdministration
vironmental
OF COMMERCE1969) forthisstudy
DEPARTMENT
GAZETTE
show that in July 1969, freakshowersoccurred,
producingover 0.75 inch of precipitationat the
collectionsite. This was followedby 0.5 inch of
rain in Septemberand over 1 inchin November.
Because of the coincidenceof normal rainfall
cycles with cambial activation,and the unusual
withpartialreactivationof
late-yearprecipitation
the cambiumbeginningin September,it is apparentthatavailabilityofmoistureplaysan important
rolein cambial activity.Duringthe same growing
season, cambial reactivationin late summerdid
notoccurin Juniperuscalifornica,a treegrowing
LITERATURE
ABBE, L. B., and A. S. CRAFTS. 1939. Phloem of white pine
and other coniferous species. BOT. GAZ. 100:695-722.
ALFIERI, F. J., and R. F. EVERT. 1968. Seasonal development
of the secondary phloem in Pinus. Amer. J. Bot. 55:518-528.
. 1973. Structure and seasonal development of the secondary phloem in the Pinaceae. BOT. GAZ. 134:17-25.
ALOSI, M. C., and F. J. ALFIERI. 1972. Ontogeny and structure
of the secondary phloem of Ephedra. Amer. J. Bot. 59:818827.
ANDERSON, B. J., and R. F. EVERT. 1965. Some aspects of
phloem development in Quercus alba. Amer. J. Bot. 52:627.
(Abstr.)
BAILEY, I. W. 1949. Origin of the angiosperms: need for a
broadened outlook. J. Arnold Arboretum 30:64-70.
BANNAN, M. W. 1955. The vascular cambium and radial growth
in Thuja occidentalis L. Can. J. Bot. 33:113-138.
BEHNKE, J. D., and G. S. PALIWAL. 1973. Ultrastructure of
phloem and its development in Gnetum gnemon, with some
observations on Ephedra campylopoda. Protoplasma 78:305319.
BENSON, L. 1957. Plant classification. Heath, Boston.
CHEADLE,
V. I., E. M. GIFFORD, JR., and K. ESAU. 1953. A
staining combination forphloem and contiguous tissues. Stain
Technol. 28:49-53.
DERR, W. F., and R. F. EVERT. 1967. The cambium and seasonal development of the phloem in Robinia pseudoacacia.
Amer. J. Bot. 54:147-153.
EVERT, R. F. 1962. Some aspects of phloem development in
Tilia americana. Amer. J. Bot. 49:659. (Abstr.)
in the same area (KEMP and ALFIERI
1974). Ap-
parentlythe amountof precipitationwas enough
to induce additionalcambial activityin Ephedra
(a low-lyingbush) but not in Juniperus.
CITED
. 1963. The cambium and seasonal development of the
phloem in Pyrus malus. Amer. J. Bot. 50:149-159.
EVERT, R. F., C. H. BORNMAN, V. BUTLER, and M. G. GILLILAND. 1973. Structure and development of the sieve-cell
protoplast in leaf veins of Welwitschia. Protoplasma 76:121.
GRILLOS, S. J., and F. H. SMITH. 1959. The secondary phloem
of Douglas-fir. Forest Sci. 5:377-388.
KEMP, R., and F. J. ALFIERI.
1974. Seasonal phloem development in Juniperus californica. Amer. J. Bot. 61:5 8. (Abstr.)
PEARSON, H. W. 1929. Gnetales. Cambridge University Press,
London.
SASS, J. E. 1958. Botanical microtechnique. 3d ed. Iowa State
College Press, Ames.
SPORNE, K. R. 1965. The morphology of gymnosperms. Hutchinson, London.
THOMPSON, W. P. 1912. The anatomy and relationships of the
Gnetales. I. The genus Ephedra. Ann. Bot. 26:1077-1104.
. 1919. Companion cells in bast of Gnetum and angiosperms. BOT. GAz. 68:451-459.
TUCKER, C. M. 1968. Seasonal phloem development in Ulmus
americana. Amer. J. Bot. 55:716. (Abstr.)
TUCKER, C. M., and R. F. EVERT. 1969. Seasonal development
of the secondary phloem in Acer negundo. Amer. J. Bot.
56:2 75-284.
SCIU.S. DEPARTMENT
ENVIRONMENTAL
OF COMMERCE,
ENCE SERVICES
ADMINISTRATION.
1969. Climatological
California. Environmental Data Service 73:216-269,
336, 380-406.
This content downloaded from 210.212.93.44 on Mon, 3 Nov 2014 07:19:22 AM
All use subject to JSTOR Terms and Conditions
data:
312-