Amer. J. Bot. 62(8):
856-868. 1975.
SEEDS AND EMBRYOS OF ARAUCARIA MIRABILIS'
RUTH A. STOCKEY
Columbus 43210
Departmentof Botany,The Ohio State University,
A B S T RA CT
cone Araucariamirabilisfrom
Seeds and embryoscontainedwithinthe silicifiedovuliferous
the Cerro Cuadrado petrifiedforestare described.One winglessseed, 0.8-1.3 cm in length
and 0.2-0.6 cm in width,is embeddedin each ovuliferousscale. Seeds show a three-layered
wavy nucelluswhichis attachedbasally to the endotesta.The
and a prominent
integument
containscellularinclusionsthatmay representstarchgrains. Ovule vascumegagametophyte
larizationis complexand appearsmostsimilarto thatof Araucariabidwillii.Embryos2 mm
long and 0.25 mm wide appear to be in a telo-stageperiodof development.Shoot apex, cotare presentin the embryosin which vascular
yledons,root meristem,and calyptroperiblem
at the time of fossilization.
tissuesand secretoryelementswere beginningto differentiate
taxa.
Embryoontogenyis consideredin lightof stages encounteredin extantgynmosperm
phase in the Cerro Cuadrado collectionis discussed.
The absence of the microgametophyte
SILICIFIED
CONIFEROUS
remainsfromthe Cerro of the BritishMuseum. She reviewedthe litera-
Cuadrado petrifiedforestin Patagonia have been
scattered to various universitiesand museums
around the world. These fossil cones, seedlings,
and wood fromthe volcanic peaks of Cerro Cuadrado, Cerro Alto, and Cerro Madre e Hija have
been sold in Argentinaas curios and kept in
private collectionsbecause of their beauty and
excellent preservation (Wieland, 1935). The
Cerro Cuadrado petrifiedforestof southernArgentina was initiallydescribed by Windhausen
(1924) who firstcollected silicifiedwood and
cones in 1919 and 1922. The collection was
passed on to ProfessorGothan (1925, 1950) of
Berlin who later describedsome of these specimens. At about the same timea second large collectionwas made by membersof the Field Museum (Chicago) of Natural History'sPatagonian
expedition (Riggs, 1926). This collection of
wood, seedlings,and cones was later reviewed
by Wieland (1929, 1935) and incorporatedin
the Field Museum collections. A few yearslater
Dr. Franz Mansfeld collected and purchased
many specimenswhile on a fossil vertebrateexpeditionin 1936 (Gordon, 1936; Calder, 1953).
Calder (1953) has providedthe most critical
studyto date of these fossilsfromthe collections
I Receivedfor publication5 September1974.
as a thesisin partialfulThis researchwas submitted
for the degree of Master
fillmentof the requirements
of Science in the Departmentof Botany,Ohio University. The authorwishes to expressappreciationto Dr.
Thomas N. Taylor for his guidance and supervision
duringthis study;Dr. Eugene S. Richardsonand the
Field Museum of Natural Historyin Chicago for making the material available for investigation;and W.
and G. W. Heien, Departmentof Geology,
Wethington
data. Supported
for x-raydiffraction
Ohio University,
in part by NSF grantGB-35958.
ture on the Cerro Cuadrado petrifiedforestand
presentedreviseddiagnoseson twigsand branches
(Araucarites santaecrucis [Speg.] Calder) and
cones (Pararaucaria patagonica Wieland, Araucaria mirabilis[Speg.] Calder).
The silicifiedovuliferouscone Araucariamirabilis (Speg.) Calder was firstdescribedby Spegazzini (1924) as Araucaritesmirabilis.Wieland's
(1935) reviewestablishedseveralspecies of cones
belonging to the genus Proaraucaria. Calder
(1953) undertooka more detailed studyof the
cones since Wieland's work was done mainlyon
the gross morphologicallevel and failed to emphasize anatomical details. She emended the
original diagnosis and also included Proaraucaria mirabilis(Speg.) Wieland,P. elongataWieland, P. patagonica Wieland, P. mirabilisvar.
minimaWieland, and P. mirabilisvar. elongata
Wieland under the binomialAraucaria mirabilis,
concludingtherewere no anatomical differences
to separate these taxa fromeach other. Calder
furthernotes that the generic name Araucaria
should be used, with Araucarites reserved for
cones or branchesof the araucarianhabit which
lack preservationof structuraldetails. Since
preserved,the
Araucaria mirabilisis structurally
generic name Araucaria is used even though
Araucariteshas taxonomicpriority.Calder has
assignedAraucaria mirabilisto the sectionBunya
Wilde and Eames (1952) that containsthe extantAraucaria bidwilliiHook., nativeto Queensland,Australia.
A shortpaper by Darrow (1936) on one cone
(P13854, Field Museum Collection) illustrated
the generalfeaturesof the embryoof Araucaria
mirabilis. Darrow principallyused polished slabs
for her investigation,
with few thin sections; the
cellularorganizationof the embryoswas not dis-
856
September, 1975]
STOCKEY-ARAUCARIA
cussed. Calder (1953) also illustrateda few embryos in her study;however,littleattentionwas
paid to cellular preservation.Detailed structure
of cones was not made available by extensivethin
in secsectioning,probablybecause of difficulty
tioningand grindingthe silicifiedmaterial. Moreover, an ontogeneticsequence of embryodevelopmenthas never been attemptedfor the fossil
cone, nor have tissuesand meristemsof the cellulary preservedembryosbeen illustrated.It is
the intentof this paper to provide a more detailed analysis of the cones with particularemphasis directedat seeds and embryos.
MIRABILIS
857
which
suggested. Since thereis an unconformity
separates this particularseries of volcanics from
the sedimentsknown to be Late Cretaceous in
age, the forestis at least as old as Middle Cretareceous. Feruglio (1949, 1951) has extensively
viewed the problem of the geologic age of the
petrifiedforestand considersthe volcanicsin this
regionto be Middle to Late Jurassicin age. His
-between
conclusionswere based on correlations
fossil plant compressions(Hausmannia Dunker,
Cladophlebis Brogn., and others) in nearby regions which he correlatedwith the Cerro Cuadrado remains. An additionalbit of evidencefor
the Jurassicage of these plants is the presence
of the branchiopod genus Cyzicus Audouin
(= Estheria) in the series of volcanics. Cyzicus
draperi(Jones) Audouin is generallyaccepted as
being Late Triassic in age (Feruglio, 1949).
presentstudy
MATERIALS AND METHODS-The
utilizes87 cone specimensassignableto the fossil taxon Araucaria mirabilison the basis of exwere selected for
ternalmorphology.Fifty-three
sectioningon examinationof previouscuts made
DESCRIPTION-General features-Cones are
by Wieland (1935) and Darrow (1936). External featuresof uncut cones, as well as those nearlysphericalto ellipsoid in shape and range
showing already exposed embryos, were con- from2.5-8 cm in lengthand 2.5-8 cm in diam
sidered before mountingthe specimensfor sec- (Fig. 1, 4, 8). Numerousspirallyarrangedcone
scales surrounda centralaxis. Each cone-scale
tioning.
The cones are completelysilicifiedby a-quartz, complex is composed of an ovuliferousscale
as determined by x-ray diffraction. Darrow whichoverliesa woody wingedbract (Fig. 1, 2).
(1936) points out the tendency for different In some cones the woody bract apophysis, or
seed tissues. outerswollen portionof the bract,is coveredby
colors of quartz to replace different
Embryos and seeds appear to be replaced by a deciduous laminar tip, which has dropped off
chalcedony,but the lumen once occupied by the in most specimens (Fig. 8). Calder (1953, P1.
nucellus is filled with transparentquartz. None 2, Fig. 40) illustrateswhat she believesto be the
of the Field Museum cones are embedded in abscissionzone of the laminartip. The presence
volcanicash, as occursin some of theBritishMu- of such a deciduouslaminartip occurs on extant
seum specimens (Calder, 1953, P1. 3, Fig. 26). araucarian cones, for example, in A. angustiSlides were made with2 x 3 in. double weight folia (Bertol.) 0. Ktze. (= A. brasilianaRich.)
glass. One side of theslide was frostedand TRA- and is known to fall offwhen cones are mature
Bond 2114 WaterWhiteTransparentEpoxy Ad- (Pilger,1926). The ovuliferousscale is freefrom
hesive (TRA-CON, Inc., Medford, Massachu- the bractforabout half its length,the freeextensetts) was used for mountingspecimensto the sion of the scale havingbeen referredto as the
slide. Sectionswerecut and groundon a Hillquist "ligule" (Fig. 1, 6). The space between the
Thin SectionMachineto a thicknessof 20-30 mi- ovuliferousscale and the bract is called the ligucrometers.Since manytissuesof the cones show lar sulcus (Fig. 6). Cone scales rangefrom0.8littlecontrast,variousslideswerestainedin a 5 % 2.3 cm in lengthand 0.5-1.5 cm in width,inaqueous MalachiteGreen solution(Bartholomew, cludingthewing-likeextensionsof thebract. The
Matten,and Wheeler,1970) forone and one-half ligule is 0.5-0.9 cm long, 0.4-0.5 cm wide at its
min. Details of pittingon the tracheids,cells of broadest point, and 0.1-0.2 cm high when exand some integumentaryposed almost completelyto view.
the megagametophyte,
Some cones show evidence of the mode of
cells of the seeds showed a greatercontrastwith
this technique. Bismark Brown stain was also burial by exhibitingwhat appear to be scorched
re- areas, pittingof the bractapophysesand ovulifertried on several sectionswithoutsatisfactory
ous scales, and distortionsdue to crushingprior
sults.
to silicification.One specimen(P13896, Fig. 4)
(1953) has pointedout shows the chalaza of severalexposed seeds. SecSTRATIGRAPHY-Calder
that the geologic age of the petrifiedforestof tions of this cone reveal that no tissues of the
preservedexcept the woody
Patagoniais stillnot accuratelydetermined.Mid- cone are structurally
dle Triassic (Windhausen,1924, 1931; Wieland, bract-and ligule tissues and some poorly pre1935; Gothan, 1925), Jurassic(Feruglio, 1949, servedsecondaryxylem. Many cones whichshow
1951; Calder, 1953; Menendez, 1960; Archan- pittingof theirouter surfacesreveal littlestrucgelsky,1970), Cretaceous (Mansfeld,in Gordon, tural detail in the firstfew cuts; however,suc1936), and Eocene (Frenguelli, 1933; Darrow, cessive cuts indicate these to be some of the
1936; Fossa-Mancini, 1941) ages have all been best preservedspecimenswithrespectto seed and
858
AMERICAN JOURNAL OF BOTANY
[Vol. 62
embryotissues(Fig. 18). Many cones are entire, 1955). Many seeds are loosely held in place in
but most are pieces rangingfrom1/4 to '/4 of a some of the more porous fossil specimens and
completecone.
oftenfall out when the cones are sectioned.
Pieces of cone pedunclerangefrom0.8-1.2 cm
are composed of threetissue
Seed integuments
in diam and 1.1 cm in lengthin some specimens layers rangingup to 1.0 mm in thickness. The
but do not revealevidenceof leaf scars externally. sarcotesta,or outercoat, is oftenpoorlypreserved
The pith of the axis is wide (0.4-0.6 cm) and and rarelyfound in attachment.When present,
containsnumeroussclereids(Fig. 2). The vascu- thislayeris mostoftenpeelingor separatingfrom
lar systemconsistsof fused bundles that forma the middlestonylayer of the seed (Fig. 14). In
continuousringin the cone peduncle. At higher places where sarcotestalcells are preservedthey
levels thisringseparatesto formdiscretebundles appear to be in layersof 3-4 cells, with each of
cells about 15 x 75
that surroundthe pith. These bundles are sur- the elongateparenchymatous
rounded by what Calder (1953) refersto as a micrometers.The sarcotestais continuouswith
"sheath of extra-phloemtissue"; however, in- the ovuliferousscale tissuesin whichthe seed is
dividual phloem cells are not usually preserved. embedded.
The sclerotesta,or middlelayer of the integuThe vascular supplyof the cone-scale complexis
double at its source; a lower and an upper in- ment,is 355-715,um thick (Fig. 14). In tanverted series of vascular bundles pass out into gential section the elongate, often branched
thebractapophysisand laminartip and theligule, sclereids show a zig-zag pattern of orientation
respectively.These vascular strandsare accom- which is presentfromthe chalaza to the micropanied by resin canals which are lined by an pylar end of the seed (Fig. 10). These thickepithelium(Fig. 5, 11). The ligule is strongly walled cells are oftenbranchedand may be 150
vascularized by six bundles of short tracheids lumlong. Sclerotestalcells become more elonregionwherethelayer
which have alternate,multiseriatebordered pits gate towardthemicropylar
on theirradial and tangentialwalls. The vascu- is thinnestand are thickestat the seed chalaza.
lar bundles in the bract are each underlainby These cells generallyformthe micropylarlining
a resin canal which accompaniesthe bundle into (Fig. 15). Araucarianseed micropyleshave been
the deciduous laminar tip. The presence of described as "mouth-shaped"in transversesecwinged cone scales and a stronglyvascularized tion (Burlingame,1915), and thisfeatureis also
ligule free fromthe bract has promptedCalder evidentfor the seed of Araucaria mirabilis(Fig.
(1953) to put A. mirabilisintothe sectionBunya 15).
is referredto as
The thirdlayer of integument
of the genus Araucaria.
In general, the cones of Araucaria mirabilis the endotesta. This layer averages about 150,um
are very sclerotic;sclereidsor fibershave been in thicknesswhen present;however,the cells of
observedin the pith,"ligule,"bract,seed integu- this tissue are rarelypreserved. This innerlayer
ments (sclerotesta), and scatteredin corticalre- of integumentis composed of parenchymatous
gions of the cone axis. The cones appear to have cells 65-80ktmin diam (Fig. 14).
numerousresin canals in the cortex,ovuliferous The nucellusis freefromthe enclosinginteguscale, bract apophyses,and perhaps in the pith, ment except in the chalazal region where it is
but never in the secondaryxylem of the cone fusedto theinnerlayerof theseed coat (Fig. 14).
It appears stalked as Eames (1913) has shown
peduncle.
in Agathisaustralis(Lamb.) Steud. and referred
Seeds-Seeds measure 0.8-1.3 cm in length to as "stipitate." The nucellar apex is wavy in
and are 0.2-0.6 cm wide (Fig. 11). One wing- outline and appears to be tenuouslyfolded and
less seed is embedded in each ovuliferousscale, invaginated(Fig. 11, 12). Darrow (1936) sugwiththe micropyledirectedtowardthe cone axis. gestedthis foldingwas probablydue to crushing
No instanceswere encounteredwhere there was or digestionby pollen tubes. In severalseeds the
morethanone seed per scale as is thecase in some nucellushas been foundextendingintothe microlivingaraucarians(Mitra,1927; Wilde and Eames, pyle and stillappears cellular (Fig. 12). In most
Fig. 1-10. Araucariamirabilis.a, cone axis; ap, apical initials;b, bract;c, cortex;co, corpusor centralmother
cell group;cot, cotyledon;1, ligule; ls, ligularsulcus; os, ovuliferousscale; p, pith;pv, provascularstrand;r, resin
canal; rm,rib meristem;s, seed; scl, sclerotesta;t, laminartip;vb,vascularbundle;w, wing;x, xylem. 1. External
surfaceof ovulatecone. P13852. X 1. 2. Transversesection of cone in peduncleregion. P13929 #1. X 4.2.
3. Tracheidswithcircularborderedpits in ovuliferousscale vascular bundle. P13888 #1. X 170. 4. External
surfaceof cone showingexposed seeds. P13896. X 1. 5. Transversesectionof bract apophysis.P13929 #1.
X 15.7. 6. Longitudinalsectionof cone, showingovules and ovuliferousscales. P13820 11 A #1. X 7.4. 7.
Longitudinalsectionof embryoshoot apex. P13816 #4. x 275. 8. Externalsurfaceof cone,showingdeciduous
laminartip. P13825. X 1. 9. Vascularbundlesin regionof seed chalaza. P13888 #1. x 26.8. 10. Tangentialseccells. Arrowindicatesbranchedsclereid. P13885 #2. X 162.
tionof seed integument
sclerotestal
September, 1975]
859
MIRABILIS
STOCKEY-ARAUCARIA
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AMERICAN JOURNAL OF BOTANY
[Vol. 62
seeds, however,the nucellus is thin and appears down extendingto the middle of the megaspore
lignified(Fig. 16, 18).
cavity. The cells appear long and tube-likeand
Traces have been found of what may be the have been referredto as "alveoli" (Chamberlain,
remnantsof the megasporemembrane.It is usu- 1935). Subsequent divisionsbreak up the "alally crushedand discontinuous.The scantypres- veoli" into smaller cells. The resultingmegaervationof the megasporemembraneis probably gametophyte
showsa regulararrangement
of cells.
due to the factthatit was not an intactstructure Since the megagametophyte
cells of A. mirabilis
because of megagame- showno evidenceof "alveoli,"wall formation
at the timeof petrification
may
tophyte and embryo expansion. Thomson have been similarto thatof Pinus.
(1905b), Eames (1913), and Burlingame(1915)
The absence of cell walls in Araucaria mirabiall commenton the thinand poorlydifferentiatedlis megagametophyte
tissue is probably due to
megasporemembraneof Araucaria compared to theirthinand delicatenature. Burlingame(1915),
that,for example, of Agathis,which has a cap- in a study of A. angustifolia(= brasiliensis),
like structureformedover the top of the mega- notes the delicate nature of megagametophyte
gametophyte.This cap presumablyforcespollen cell walls as well as difficulty
in photographing
tissue from the tissuebecause of the numerousstarchgrains.
tubes to enterthe megagametophyte
the sides, thus preventingthe destructionof the
One megagametophyte
(P13892 #4) contains
(Eames, 1913). what may be two sunken archegonia (Fig. 19).
upperportionof thegametophyte
When extant araucarian seeds are mature, the These consistof two ellipticalcavitiesin theupper
megaspore membrane is not usually visible portionof the megagametophyte
tissue on either
(Thomson,1905b).
side of themicropylar
canal. No neck cells or any
is presentin cellular preservationinside the cavities was obTissue of the megagametophyte
most seeds and is fullydeveloped,fillingmost of served. The natureof jacket or othersurroundthe nucellar cavity (Fig. 11, 16, 18). Mega- ing cells is unknown. These ellipticalcavitiesnot
gametophytetissue commonlyreaches a length only appear to be in the appropriatepositionto
of 0.5 cm and a widthof approximately0.2 cm. be araucarianarchegoniabut, moreover,are of a
The cells are isodiametricand 50-70 ,m in diam. uniformsize and shape. They appear to be simiIn most seeds the delicate cell walls are not pre- lar to those described by Eames (1913) for
served but are representedby what appear to Agathis australis, which are produced superfihave been cellular inclusions or contents. A cially,near the surfaceof the megagametophyte,
granular matrix with small spherical bodies is and by a subsequentproliferationof the megathatmeasure gametophytetissue become sunken.
sometimesvisible. These structures,
3-5 ,m in diam, appear to be slightlyangularin
Vascularizationof the ovule is complex and
cells correspondsto some extentwiththe vascularsysoutline (Fig. 17). The megagametophyte
selectivelytakeup theMalachiteGreenstainmore tem thatWilde and Eames (1948) show for the
consistently
than othertissuesof the seed or em- seed of Araucaria bidwillii.Vascular bundlesare
bryo. Cells in contactwiththe embryoappear to extensiveat the chalaza of the ovule, with 1-4
be flattenedslightly;those towardthe micropylar bundlespresentin the ovule bases (Fig. 14). A
end of the seed are more elongate. Althoughno seriesof six vascularbundlesentersthe tip of the
tissuehave ovuliferousscale (Fig. 13). Worsdell(1899) reovules witha solid megagametophyte
been foundin which no embryois present,wall ports "concentricbundles" in the ligule of A.
tissue bidwillii,each with spiral thickenings,although
formationin A. mirabilismegagametophyte
may have been of the Pinus type (Chamberlain, he never notes the actual number of bundles.
forma- Vascular bundles,oftenwiththe protoxylemele1935). In this type of megagametophyte
the ments surroundedby a ring of metaxylemtration cell walls are laid down centripetally,
periclinalwalls being the last to be laid down. cheids, are typicalof those seen in A. mirabilis.
The resultis a randomorientationof cells and a In cone transversesections two large vascular
megagametophytewith a weak central region bundles are presentin the ovuliferousscale (Fig.
caused by the line of closurewheretwo cell walls 9). Tracheids in this region are nearly as wide
are in contact (Chamberlain,1935). The other as they are long (60-70 mm) and have altercircularborderedpits
typeof wall formationcommonin conifersis il- natelyarrangedmultiseriate
lustratedby Taxus, where the cell walls are laid on their radial and tangentialwalls (Fig. 3).
m, megaFig. 11-15. Araucariamirabilis.a, cone axis; b, bract; e, embryo;end, endotesta;int, integument;
mi, micropyle;n, nucellus;os, ovuliferousscale; r, resin canal; sar, sarcotesta;scl, sclerotesta;vb,
gametophyte;
vascularbundle. 11. Longitudinalsectionof seed, showingprincipalfeatures.P13939 #1. X 11. 12. Oblique
sectionof ovule,showingremnantsof nucellus. P13888 #1. X 18. 13. Transversesectionof bractand ovuliferous scale near regionof ligularsulcus. P13929 #1. X 29. 14. Longitudinalsectionof seed in regionof chalaza.
P13939 #1. x 35.8. 15. Transversesectionof ovule, showingirregularly
shapedmicropyle.P13939 #4. X 24.
STOCKEY-ARAUCARIA
September, 1975]
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MIRABILIS
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AMERICAN JOURNAL OF BOTANY
These two large groups of tracheidsmay representthe portionsof the upper (ovuliferousscale)
series in the cone-scale complex which Eames
(1913) referredto as "the crowded twisted
groupswhich come togetherbehind the ovule in
a horizontalseriesand pass on intothe freeligule
as strongbundles." Eames (1913) describeseight
bundles thateventuallypass into the ligule of A.
bidwillii.
Embryos-The embryosof Araucaria mirabilis appear to be in what Schopf (1943) has referredto as the telo-stageperiod of development.
Embryosare foundembeddedin themegagametophytetissue, and as Calder (1953) has pointed
out, the orientationof the plane in which the
cotyledonslies varies fromone almostparallel to
one at rightangles to the surfaceof the ovuliferous scale. Longitudinalsections of the embryo
show the typicalfeaturesof a conifertelo-stage
embryo: shoot apex, cotyledons,area of permanentinitialsof the root meristem,columella,and
calyptroperiblem(Fig. 7, 16, 18, 20, 23-28).
In the Cerro Cuadrado embryosthe vascular tissues are just beginningto differentiate.Darrow
(1936) has reported that there are only two
cotyledons present in the embryo, with each
reachinga lengthof about 2 mm and a widthand
depth of 0.25 mm (Fig. 16, 18, 26-28). Each
cotyledonis supplied by six provascularstrands
(Fig. 26).
Calder's (1953) figuresof A. mirabilisembryosshow what appears to be cellularpreservation althoughshe never makes note of this fact.
Most embryosdo not show preservationof the
delicatecell walls. Each cell is representedin the
embryoby a small sphericalbody 5-6.5 ym in
diam (Fig. 7). In embryoswhere cell walls are
preserved,one of thesesphericalbodies is present
in each cell (Fig. 21). They become more elongate in the regions of the provascular strands,
where theymeasure 17 x 2[tm. These spherical
bodies or inclusionsin the cells of the embryos
provideexcellentmarkersfor the tissue zones of
the telo-stageembryo. Their possible originsin
the livingembryomayhave been proteingranules
or globules, starchgrains,or some other stored
material. They may also representnuclei, since
thereis only one per cell, and theyare elongated
[Vol. 62
in the provascularregions. Living nuclei in differentiating
xylem elementsare oftenlarger and
more elongate than nuclei in cells where differentiationis not occurring(Scott, 1940).
The shoot apex has a diam of 112-135,m and
appears to have a surfacemeristemcomposed of
a layerof apical initials. Some apices show what
appear to be two surfacelayers. Griffith(1952)
reportsa discretesurfacelayeror tunica in living
araucarian shoot apices. In two species (Araucaria araucana [Molina] K. Koch [= A. imbricata
Pavon] and A. bidwillii) a second discretelayer
is presentin '90 % of the shoot apices; sometimes
more than two surfacelayers are found in these
species. Embryos of A. mirabilisshow one and
whatmaybe two surfacelayersof cells. In apices
with a so-called tunica-corpusarrangementof
the meristem,the numbers of parallel surface
layersmay vary duringthe ontogenyof the plant
and also with seasonal growthchanges (Romberger,1963; Griffith,
1952). The centralmother
cell group of most gymnospermsunderlies the
surfacemeristem(Romberger,1963). This region is referredto as the corpus in angiosperms,
Gnetum, and Araucaria (Griffith,1952; Romberger,1963). In A. mirabilisthereis a corpuslike region beneath the surfaceinitialsin which
thereis a more or less randomorientationof cells
(Fig. 7). No leaf primordia,like those that occur in the dormantstage of some gymnospermous embryos(Buchholz and Old, 1933), have
been observed. Beneath this corpus-likearea is
the rib meristemin which the cells are oriented
in longitudinalrowsthatin livingmeristemsshow
a gradualmaturationaway fromthe apex to form
pith cells. The longitudinalrows of cells which
make up the centralcolumn or hypocotylregion
of A. mirabilisembryosare veryprominent(Fig.
20), and the hypocotylregion extends for a
lengthof 1.2 mm (Fig. 16).
The generativemeristemof the root is representedby a group of permanentinitials(Fig. 18,
20). Beneath this region of initialsthe column
or columellarregionextendsfor a lengthof 1.2
mm (Fig. 16, 20). This temporarymeristematic
region adds cells to the "root cap" by periclinal
divisions (Allen, 1947). The "root cap" or calyptroperiblem
region (Buchholz and Old, 1933)
measures about 1.1 mm x 0.9 mm and extends
Fig. 16-22. Araucaria mirabilis. ar, archegonium;cal, calyptroperiblem;
cc, centralcolumn; col, columella;
cot, cotyledon;cw, cell wall; end, endotesta;gm, generativemeristemof the root; h, hypocotyl;i, inclusion;m,
megagametophyte;
mi, micropyle;n, nucellus;pi, permanentinitials;pv, provascularstrand;sa, shoot apex; sb,
sphericalbodies; scl, sclerotesta;su, suspensorremains. 16. Longitudinalsectionof telo-stageembryoand surroundingtissues. P13816 #4. X 22.3. 17. Cells of the megagametophyte,
showing inclusions. P13865 #2.
X 295.7. 18. Longitudinalsectionof embryocontainedwithinseed. P13865 #3. x 14. 19. Oblique sectionof
megagametophyte
tissue,showingpossible sites of archegonia.P13892 #4. X 59.5. 20. Longitudinalsectionof
embryoroot meristematic
region. P13816 #3. X 42. 21. Cellular organizationof the embryo. P13816 #3.
X 269. 22. Longitudinalsectionof seed, showingsuspensorremainsin micropylarregion. P13892 #3. X 60.2.
STOCKEY-ARAUCARIA
September, 1975]
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AMERICAN JOURNAL OF BOTANY
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[Vol. 62
September, 1975]
STOCKEY-ARAUCARIA
for about '4 of the embryoproper (Fig. 16, 18,
20, 25). At the basal portionof the embryothe
calyptroperiblem
is jagged in outline, probably
indicatingthe place of detachmentfromthe suspensors(Fig. 16).
Beneath the protodermof the embryo,and in
the cortex, is a ring of 12 secretoryelements,
resinducts,or canals which also extendinto the
cotyledons(Fig. 24, 27, 28). Darrow (1936)
makes a briefnote of theirpresencein one of her
text figureexplanations. Individual canals measure 25-40 1,min diam. Burlingame(1915) has
reportedtwo such ringsof resinductsin the cortex and pericycleof A. angustifolia. Only one
ringhas been observedin the cortexof the embryosofA. mirabilis.
The remains of highlycoiled suspensorscan
be seen in various planes of section (Fig. 22).
In only one seed were the suspensorsseen to be
stretchedout and more or less uncoiled or
straight.This may be an embryoin an earlier
stageofdevelopment.
Figures 23-28 are a series of transversesectionstaken at variouslevels of the telo-stageembryo. Figure 25 is a section taken somewhere
withinthe columellarregion. Cells convergetoward a centralpoint, the column or columellar
region, where calyptroperiblemcells originate.
A section a littlefartherup the embryoin the
hypocotylregionshows thatthe vascular cylinder
is split into two C-shaped strands (Fig. 24).
These two C-shaped strands each divide at a
higherlevel to produce four strands (Fig. 23,
24). At a stillhigherlevel each dividesto forma
totalof six strandsthatenterthe cotyledons(Fig.
26, 27, 28). Figure 28 is a section taken at a
plane which crosses the shoot apex region and
Fig. 27 at a level just above the point of cotyledonary divergence. Cotyledons themselvesextend for about 1/2 of the embryoproper.
DISCUSSION-The fossilovulatecones of Araucaria mirabilisshow the greatestresemblanceto
extantspecimensof A. bidwillii(section Bunya).
Calder (1953) reportsthatthe stronglyvascularized ligule (freeportionof the ovuliferousscale)
and the separate originsof bract and ovuliferous
scale vascular supplies seem to ally A. mirabilis
withthis species. This patternof vascularization
is onlyfoundin the sectionBunya (Eames, 1913;
Aase, 1915; Wilde and Eames, 1948, 1952).
Darrow (1936) points out the similarityof the
embryoof A. mirabilisto that of A. bidwilliiin
MIRABILIS
865
the presenceof two cotyledons. Cotyledonnumber in the genus ranges from 2-4 (Butts and
Buchholz,1940). Darrow (1936) also compares
the embryoto those of A. araucana and A. angustifoliain which the hypocotylconstitutesless
thanl, of the totalembryolength.She statesthat
the fossil embryo has a hypocotylthat comprises about half of the embryoproper. The thin
sectiontechniqueused in this studyhas demonstratedthat the regionfromshoot apex to point
of suspensorattachment
is about 1/2 of the embryo
proper;the otherhalf is comprisedof the cotyledons. The actual hypocotylconstitutesabout '4
of the embryoin A. mirabilis,the calyptroperiblem or "root cap" regionabout one fourth.
The diameterof the shoot apex in araucarians
varies from 116 /m in Araucaria cunninghamii
Ait. ex Lamb. to 168 1,min A. araucana (Griffith,1952). The apex of A. mirabilisreaches a
diam of 135 /m, thus showinga similarityto the
apex of A. bidwillii,whichreaches 134 /m (Griffith, 1952). There appears to be one discrete
layer of apical initialsand perhaps two in some
apices, as is seen in A. bidwilliiand A. araucana
(Griffith,
1952).
The greaterdepth of the ligularsulcus (space
betweenovuliferousscale tissue and that of the
bract) in A. mirabilisas comparedto thatfeature
in other araucarian cones prompted Wieland
(1935) to institute the genus Proaraucaria.
Wilde and Eames (1948) point out that at a
stage about 3 weeks afterpollinationthe ovuliferous scale is stillfreeforabout halfits lengthin A.
bidwillii;later the lengthof the fusedportionincreases. Calder (1953) suggestedthat the depth
of the sulcus alone was not enough to justifya
new genusforthefossilcone.
arauVishnu-Mittre
(1954) describeda petrified
carian cone, AraucaritesbindrabunensisVishnuMittre,fromthe Jurassicof India. This cone resembles A. mirabilisin several respects and is
regarded as an extinct species of the section
Bunya. One reasonfortheseparationof thiscone
fromAraucaria mirabilisis the presenceof longer
scales and seeds. It should be noted that the
range of measurementsin seed and scale length
in A. mirabilis,as reportedhere,coversthe range
found for Araucarites bindrabunensis.Cells of
the pithin most cones of Araucaria mirabilisare
not sufficiently
preservedto determinethe presence of resincanals, whichare reportedin Araucaritesbindrabunensis.Also, in Araucaria mirabilis many bract apophysesin' certainsections of
versesectionof embryoin hypocotylregion. P13925 #7. X 63. 24. Transversesectionof embryoin hypocotyl
region,showingC-shapedstrands.P13853 #4. X 49. 25. Transversesectionof embryoin columellarregion.
P13925 #6. X 147. 26. Transversesectionof embryocotyledons,showing6 vascular bundles. P13925 #7.
divergence.P13925 #6. x 44.3. 28.
x 38. 27. Transversesectionof embryojust.above pointof cotyledonary
Transversesectionof embryoat pointof cotyledonary
divergencewith6 vascularbundles. P13925 #7. X 49.
866
AMERICAN JOURNAL OF BOTANY
[Vol. 62
tangentialcuts do not readilyshow the presence whereas those of Agathis (Eames, 1913), as in
of resin canals (Fig. 2, 13). Vishnu-Mittre's most conifers,maturein threeyears.
have not been obConditionsof polyembryony
drawingof cross sectionsthroughcone scales appears much like similarsectionsof A. mirabilis, servedin A. mirabilissince most of the seeds are
at relativelythe same stage of development.The
especiallywith respectto vascularization.
nature of the embryoniccap of cells characterWilde and Eames (1955) and Mitra (1927)
cone istic of proembryosof Araucaria and Agathis
have suggestedthat studiesof multi-ovulate
scales may indicatethat the one seed per cone- has been much speculated upon (Strasburger,
scale complexfeatureof araucariansis a derived 1872; Seward and Ford, 1906; Eames, 1913;
conditionfromtwo or three ovulate types. No Buchholz, 1920). Buchholz (1920) has sugscales bearingtwo or three seeds have yet been gestedthe cap functionedin preventingcleavage
foundamongthe cones of A. mirabilis.The one- polyembryony.OthersincludingEames (1913),
seed condition seems to have evolved in the Seward and Ford (1906), and Strasburger(1872)
Araucariaceae at least as early as the Jurassic. have suggestedthatthe cap functionedin protecThe oldest known fossil embryohas been de- tionof the embryo.Buchholz (1920) regardsthe
scribedby Miller and Brown (1973) in a voltzia- functionof the cap for the secretionof enzymes
lean cone (Moyliostrobustexanum Miller and as a remotepossibility.The presence of a cap
Brown) fromthe Permianof Texas. This Paleo- or detailsof its formationare not available in the
zoic embryo consists of an elliptical area of embryoof Araucaria mirabilisat this time.
parenchymawiththreetracheidscontainedwithin
Buchholz (1919) has suggestedthe evolution
the megasporewall. The Moyliostrobusembryo of dicotyledonyfrom a polycotyledonouscondiseems to be at a later stage of developmentthan tion. He states that the fusion of cotyledonary
that of Araucaria mirabilissince-tracheidswith primordiain Pinus banksianaLamb. and Cedrus
annular and spiral thickeningsare already dif- libani A. Rich. in the early stages of cotyledon
ferentiated.Tracheidshave not yet differentiatedelongationor the abortion of cotyledonarypriin the arau- mordia may show a manner in which dicotyleand laid down secondarythickenings
no megagameto- dony may have arisen. Araucaria mirabilisemcarian embryo. Unfortunately,
phytetissuewas foundin theMoyliostrobusseeds. bryos in earlier stages of developmenthave not
In Araucaria mirabilis,however, megagameto- been found showing only cotyledonaryprimorphytecells are presentand cellularcontentssug- dia, and consequentlytheirnumberis unknown.
gestedby the presenceof a granularmatrixand However, the dicotyledonouscondition of the
roughlyangular to spherical cellular inclusions araucarian telo-stageembryo is presentby the
which may be starch grains or protein bodies Jurassicperiod.
The lack of pollen cones has likewise been
(Fig. 17).
Most embryosof A. mirabilisshow the typical speculatedupon by Calder (1953). She believes
telo-stageconditionthat is common in conifers theirabsence is due to the season in which the
(Fig. 16). Schopf (1943) has suggestedthatthe forestwas covered. Perhaps evidence of them
may be in- will yet be found in the volcanic ash matrix.
monophyleticoriginof gymnosperms
dicated by the apparent similarityof nearly all Menendez (1960) described a pollen cone,
embryosat the telo-stageperiod, MasculostrobusaltoensisMenendez,fromthe regymnospermous
even thoughthe various groups show differences gions around Cerro Alto. His work dealt with
in vegetativehabitas well as in earlystagesof em- four cone specimenscontainingsphericalpollen
bryo development. The great similarityof the grains 100-120 /umin diam. Sufficientdetails of
telo-stageembryoof Araucaria mirabilisto that anatomywere not presentto assign the cones to
of otherconifersindicatesthat this stage of de- any of the major coniferfamilies. These cones
velopmentwas presentin conifersas early as the may representthe pollen cones of Araucaria miJurassic.
rabilis,Pararaucaria patagonica, or perhaps anThe presence of no earlier stages in embryo othergymnosperm
foundin the Cerro Alto forest.
developmentin A. mirabilismay be due to the As Menendez (1960) and Calder (1953) point
time and mode of preservationof the forest. If out, the cones in the Field Museum collections
the forestwas covered by volcanics while most consideredby Wieland (1935) to be "staminate"
cones showedtelo-stageembryos,and the smaller are actuallysmaller ovulate cones. No other of
newlyformingcones were just developingovules, the collectinglocalitieshas reportedpollen cones
the resultantfossilsmay be reflectedin what is buttheCerroAlto region.
There is also a lack of pollen tubes or pollen
seen in the Cerro Cuadrado remains. Calder
the
fossil
attention
to
on, or embeddedin, tissuesof the ovulate
also
calls
seedlings
grains
(1953)
in the collectionto point out threegenerationsof cone of A. mirabilis. Their absence is most puzremains withinthe petrifiedforest. Burlingame zling in light of the strongerosive capacity of
(1913, 1914) reportsthat extant ovulate cones araucarianpollen tubes in extantspecies (Eames,
of Araucaria also take two years to develop; 1913). The pollen of Araucarialands on the ex-
September,1975]
STOCKEY-ARAUCARIA
MIRABILIS
867
tendedportionof the ovuliferousscale and grows
LITERATURE CITED
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sporophylls
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1935a, b). Eames (1913) notes that araucarian
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e.g., ovuliferousscale, cone axis, includingxylem
Cienc. Nat. Mus. Ser. Techn. y Didact. No. 11, La
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BARTHOLOMEW, R. L., L. C. MATTEN, AND E. F.
Eames (1913) suggeststhatperhapsparthenoWHEELER.
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linated have jacket cells of the archegoniathat
106-119.
break down, theircontentsbeing freed into the
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bryonyin relationto the phylogenyof conifers.
fuse and migratetoward the egg nucleus. He
Amer.J.Bot. 7: 125-145.
has also observed them indentingthe nuclear
, ANDE. M. OLD. 1933. The anatomyof the
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pressed some doubt as to the actual fusionwith
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tents occurred under normal conditionsof fergametophyte.Bot. Gaz. 55: 97-114.
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58-62.
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99-138.
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AND
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