Amer. J. Bot. 64(6): 733-744. 1977.

REPRODUCTIVE BIOLOGY OF THE CERRO CUADRADO () : PARARAUCARIA PATAGONICA

RUTH A. STOCKEY Departmentof ,The Ohio StateUniversity, Columbus 43210

A B S T R A C T Seventy-twosilicified cone specimensof Pararaucariapatagonica Wieland fromthe Cerro Cuadrado (Jurassic)petrified forest in Patagoniawere studiedby use of thinsections and re- flectedlight. Traces fromthe cone axis stele to the and ovuliferousscale are separate at theirorigins. In cross sectionthe abaxiallyconcave ovuliferousscale trace and massivecir- cularbract trace branch half-way out intothe cone-scalecomplex. Two triangular-shapedbun- dles of fibersfollow the scale trace into the laminarpart of the ovuliferousscale. Both sur- faces of the ovuliferousscale possess hairs whichmay have assistedin cone closure. Cones typicallycontain one flattened,winged seed per ovuliferousscale. Multi-layeredseed integu- mentsare representedby an innerfleshy layer of large cells filledwith a black amorphous material,a sclerotestaconsisting of wedgesor fan-shapedgroups of sclereidsoriented at right angles to the seed surface,and a thin,often crushed fleshy layer. Seed wings consistof anastomosing,branched cells resemblingglandular hairs and containingmany intercellular spaces. Well-preservedpolycotyledonous containing up to eightcotyledons are present in severalcones. Tissues of the embryoincluding the shootapex, calyptroperiblem,hypocotyl, and cotyledonsare described.On the basis of anatomicaland morphologicalfeatures, speci- mensof P. patagonicaare comparedto membersof both extantand extinctfamilies of coni- fersincluding the ,Taxodiaceae, Pinaceae, ,and Cheirolepidaceae.

THE CERRO CUADRADO petrifiedforest in Pata- known fromthe petrifiedforest and at firstwas gonia (Santa Cruz, ) was initiallyde- thoughtto representtwo distinctspecies, P. pata- scribed by Windhausen (1924). Among the gonica and P. elongata. In 1935 Wieland demon- silicifiedremains found there are twigswith leaf stratedthat the range of charactersin specimens scars,wood, supposed seedlings,and threegenera of Pararaucaria did not warrantthe recognition of coniferouscones that were deposited in place of two , since the variation within the by a (Wieland, 1935; Menendez, cones was no more than that occurringin cones 1960). Many specimens, principallycollected of extant Pinus species. This initial description from the three volcanic peaks of the region was based on 20 cone specimens of the iField (Cerro Cuadrado, Cerro Alto, and Cerro Madre Museum collection throughthe use of polished e Hija) ultimatelybecame the propertyof Amer- surfaces (Wieland, 1935). Wieland believed the ican and European museums. Among these re- cone representeda transitionform between the mains is the silicifiedovuliferous cone Pararau- Araucariaceae and the Pinaceae based on seed caria patagonica, first described by Wieland and cone-scale features,and cone vasculariza- (1929) in a preliminarytreatment of the Field tion. He placed it in the Cheirolepidaceae,a fam- Museum of NaturalHistory (Chicago) collection. ily of coniferserected by Hirmer and This cone is the smallerof the two ovulate cones Horhammer (1934) and emended by Jung (1968). 1 Received for publication21 October 1976; revision Calder (1953) emended the genericdiagnosis accepted 1 February1977. of Pararaucaria to fitthe range of variationseen The authorwishes to thankthe followingpeople for in the BritishMuseum collection and employed theirgracious loan of specimensand use of laboratory thin sectioningin additionto studies of polished facilities: Dr. Eugene S. Richardson,Field Museum of NaturalHistory, Chicago; Mr. CedricShute, British Mu- faces. Structureof the xylem in the cone axis seum of Natural History,London; Dr. Hans Tralau and was compared to extantconifer families. In ad- Dr. BrittaLundblad, Naturhistoriska Riksmuseet, Stock- dition, the presence of many cotyledonsin the holm; Dr. James M. Schopf and Dr. Stig Bergstrom, embryoand the winged nature of the seed were United States Geological SurveyCoal Geology Labora- toryand OrtonMuseum, The Ohio State University;Dr. reported. Calder placed Pararaucaria in the Francis M. Hueber, United States National Museum, Taxodiaceae because of the greatdiversity within SmithsonianInstitution. Special appreciationis expressed the (sensu Pilger, 1926) stating that it to Dr. ThomasN. Taylorfor his help and guidancedur- ing this study. Supportedin part by National Science resembledno one living in the combina- Foundationgrants BMS 75-14221 and BMS 74-21105. tionof characters. 733 734 AMERICAN JOURNAL OF BOTANY [Vol. 64

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The excellentsilica permineralizationof these cheids showed a greatercontrast with this tech- cones offersa rare opportunityto studydelicate nique. Most slides, however,were leftunstained seed and embryotissues some of whichappear to and mountedin HSR (Harleco SyntheticResin). have cellularcontents. The purpose of thispaper A numberof taxa of coniferseed wings were is to provide a detailed analysis of the cones of studied for comparison with those of Pararau- Pararaucaria with particular emphasis directed caria. These included seed wings of several gen- at seeds and embryosand to comparethese cones era of the Pinaceae, Cupressaceae, Taxodiaceae, with those of several extant as well as extinct and Agathis australis (D. Don) Salisburyin the coniferfamilies. Araucariaceae.

MATERIALSAND METHODS-The presentstudy STRATIGRAPHY-The age of the petrifiedforest utilizes72 cone specimensassignable to the fos- is still not accuratelydetermined; however, most sil taxon Pararaucaria patagonica on the basis of workerstoday follow the interpretationsof Fer- externalmorphology and previouslycut surfaces. uglio (1949, 1951) who believes that the Cerro Thirty-fivecones were selected for sectioning Cuadrado sedimentshave a Middle to Late Juras- based on examinationof previous cuts made by sic age (Calder, 1953; Menendez, 1960; Stockey, earlier workers. Material includes specimens 1975a). fromfour collections: The Field Museum of Na- tural History (Chicago), the British Museum DESCRIPTION-General features-Cones vary (Natural History) London, NaturhistoriskaRiks- in shape from conical to cylindrical,sometimes museet (Stockholm), and Orton Museum of ovoid, and are 5.1-2.3 cm long and 2.6-1.3 cm Geology (The Ohio State University,Columbus). in diam (Fig. 1). Numerous helically arranged The cones are completelysilicified and appar- cone-scale complexesare arrangedin a 3/8 phyllo- entlycontain littleor no organic material. Dar- taxyaround a slendercone axis. Each cone-scale row (1936) pointed out the tendencyof cones complex is composed of a large, woody ovulif- from these localities to display differentcolors erous scale which is subtended by a smaller of quartz replacing differentseed tissues. Em- woody, flattenedbract (Fig. 1, 2). Externally bryos appear to be replaced by chalcedony,and cone-scalesresemble those of certainmembers of the space once occupied by the nucellus is filled the Taxodiaceae, e.g., Sciadopitys Siebald and with a transparentquartz. Some cone specimens Zuccarini and Sequoiadendron Buchholz; how- appear to be more porous than others,especially ever, the bract and ovuliferousscale of Pararau- betweenthe ovuliferousscale and bract,between caria are not fused but free for almost theiren- sclereidsof the stoneylayer of the seed, and in tirelength (Fig. 3, 6). the cavityonce occupied by nucellus. Most cones In less weatheredspecimens (Fig. 2), the outer are composed- of dense a-quartz (Stockey, surfaceof the ovuliferousscale appears striated. 1975a). None of the specimensthus far observed No laminartip, umbo, or extensionof the ovulif- are known froma volcanic ash matrix,as is the erous scale into distinctlobes has been observed. case for some specimens of mirabilis Some cones show evidence of scorched areas or (Calder, 1953). pittingof the ovuliferousscales and distortion TRA-Bond 2114 Water White Transparent due to crushing,suggesting evidence of burial by Epoxy Adhesive (TRA-CON, Inc., Medford, volcanic ash. In a few weatheredcones, seeds Massachusetts) was used for mounting speci- with visible internaltissues are exposed. Only mens to the glass slides. This epoxy has a refrac- four specimens of those examined show pieces tive index (1.565) close to that of quartz thus of cone peduncle,and all of these appear to have giving excellent optical properties. Few cones poorly preservedleaves surroundingthe axis of showed littlecontrast with most tissuesappearing the type described by Calder (1953). She fig- clear-buffin color. Thin sections of these were ured one BritishMuseum specimenwith spirally stained in a 5% aqueous Malachite Green solu- arranged,broad, lanceolate leaves with striated tion (Bartholomew,Matten, and Wheeler,1970) surfaces that show a sharp transitionto fertile for 11/2 minutes. Details of pittingon the tra- scales. No cuticleremains are present.

Fig. 1-7. Pararaucariapatagonica. 1. Externalsurface of ovulate cone. 031218. X 2. 2. Externalsurface of less weatheredcone. Arrowindicates striation of ovuliferousscale externalsurface P13988. x 2. 3. Outermostpor- tionsof the cone-scalecomplex showing large cells with amorphouscontents. P139-- I #1. X 25. 4. Longitudinal sectionof the cone axis at a level of tracedivergence. P13978 A #1. X 7. 5. Transversesection of cone axis. P13961 #2. x 14. 6. Longitudinalsection of cone-scalecomplex showing position of seed. P13978 A #2. X 10. 7. Radial longitudinalsection of cone axis withuniseriate circular bordered pits of tracheids.P 139--I #1. x 250. b, bract;bt, bracttrace; c, cortex;os, ovuliferousscale; ost, ovuliferousscale trace; p, pith; s, seed; sc, sclerenchyma; w, wing; x, xylem. 736 AMERICLAN JOURNAL OF BOTAN Y [Vol. 64

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Cone axis-The pith of the cone axis is small The abaxially concave ovuliferousscale trace (0.5-0.8 mm) and oftennot well preserved(Fig. is formedby the fusion of two separate strands 5). Cells appear small, thin-walled,isodiametric thatbend 180? and resultsin the protoxylemdi- (45 Amdiam). Some apparentcellular contents rectedtoward the bract trace on the abaxial sur- and small spherical(5-6 Amdiam) structuresare face of the bundle. As the ovuliferousscale trace commoninside the best preservedcones. Larger departsfrom the axis stele it is accompanied on cells about 65 Amin diam withdark brown con- the adaxial side by two massive,triangular-shaped tents are scatteredthroughout the pith. In lon- sclerenchymastrands that follow the trace out gitudinal sections small, scattered, square-rect- into the ovuliferousscale (Fig. 5, 11). These angular sclereids up to 80 Amin diam can be sclerenchymastrands originatefrom the dissec- seen. This typeof pithstructure is similarto that tion of one mass of sclerenchymain the cortex in Taiwania cryptomerioidesHayata (Doyle and of the cone axis. They remain in a triangular Doyle, 1948). configurationabout half-wayout into the scale, Maturationof the primaryxylem is endarch. spread out laterally,and eventuallydisappear dis- There are helical wall thickeningson the inner- tally. These sclerenchymastrands contain ex- most tracheidsand these are succeeded by reticu- tremelythick-walled fibers 45 ym in diam. late pitting. Some tracheidsshow biseriate,cir- The upper and lower surfacesof the ovulifer- cular-borderedpits between the helical bands. ous scale are covered with what appear to have The wide zone of secondaryxylem is relatively been glandular trichomes. They are short cells undissectedand composed of small diametered thatoccasionally branch. Similarhairs have been (20-30 Am) tracheids (Fig. 7). Pittingon the reportedby Chowdhury(1961) on the surfaces radial walls is uniseriateand circular-bordered. of scales of Cedrus, and it is believed that they Vascular rays range from 1-5 cells high; no ray functionin cone closure afterpollination by the tracheids were observed. canals and productionof a resinous substancethat hardens growthrings are absent. Crushedcells, oftenap- to seal the cone closed. No actual resin canals pearing in radial rows to the outside of the xy- have been found in the or ovuliferous lem, may constitutea zone of cambium,second- scales of Pararaucaria. ary phloem, and cortex (Fig. 5). In the outer cortical region are groups of thick-walledfibers Seeds-Tissues of the seeds are well preserved that follow the vascularizationof the cone-scale in several specimens. One flattened,winged seed complex out into the ovuliferousscale (Fig. 5, is embedded in the upper surfaceof each ovulif- 11). erous scale (Fig. 6). Seeds are roughlyheart- shaped in outlineand about 6 mm long. Cone-scale complex-Traces to the bract and One seed per cone-scale complex is character- its associated ovuliferousscale are separate at isticof araucarians,hence, the name Pararaucaria theirorigins from the axis stele (Fig. 4). Thick (Wieland, 1935). Seed integumentsare usually woody bracts each with one large vascular trace representedby wedges or fan-shapedbundles of are characteristicof Pararaucaria. The bract is cells in transversesection (Fig. 10, 17-20). The free from the associated ovuliferousscale for integumentof the seed is multi-layered(Fig. 8) most of its lengthand is fusednear the cone axis. as is commonin the Taxodiaceae and the Cupres- Each bract trace is circularto oval in cross sec- saceae at later stages of development(Konar and tion for about half the lengthof the bract. Far- Banerjee, 1963). The innermostcells compose ther out in the bract and ovuliferousscale are an innerfleshly layer of large cells filledwith a numerous isodiametrictracheids with circular- black amorphousmaterial which may have been borderedpits linkingthe vascular strands,making a mucilage or resinous substance in the living up what Calder (1953) refersto as a bulkytrans- seed (Fig. 8). fusiontissue. The outer tissues of the bract and The stony layer of the seed is composed of scale contain large cells 120-180 ,um in diam many layers of cells (Fig. 8). The inner layer that are filled with brown amorphous contents consistsof small, rounded sclereidsin transverse (Fig. 3). Both surfacesof the bract appear to be section that measure 35 /Amin diam. They are smooth. overlain by a layer of tightlypacked radially

Fig. 8-13. Seed and cone-scalefeatures. 8. Pararaucariapatagonica, seed integument.P13979 #4. X 36. 9. P. patagonica,seed wing. Arrowindicates trichome tip. Note branchingof individualtrichomes. P13958 #1. X 170. 10. P. patagonica,transverse section of two-seededcone-scale complex. P13979 side #3. -X 12. 11. P. patagonica, tangentialsection of cone showingvasculature of cone-scalecomplex. P139--III A #2. x 22. 12. Abies grandis, seed wing surface. Arrowsindicate bulbous tips of cells. X 200. 13. P. patagonica. Arrowindicates seed abscis- sion layer.P13978 B #1. x 12.5. bt,bract trace; end, endotesta; ost, ovuliferousscale trace;s, seed; sar, sarcotesta; sc, sclerenchyma;sc, sclerotesta;vb, vascularbundle; w, wing. 738 AMERICAN JOURNAL OF BOTANY [Vol. 64

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elongate sclereids (65 ym long) whichis usually inclusionsup to 5 ym in diam. Cells do not show one cell thick. Some seeds show two layers of any evidenceof alveoli as in Taxus megagameto- radiallyelongate cells in this region. Konar and phytetypes (Chamberlain, 1935), but do show Banerjee (1963) have reporteda similartype of a regulararrangement of isodiametricthin-walled seed integumentin the extantCupressus funebris cells. This type of cell structurewould indicate in which sclerotestalcells are rounded sclereids the presenceof a Pinus typeof megagametophyte at early stages of seed developmentand become (Chamberlain, 1935). None of the seeds thus radiallyelongate with time. The formationof an far examinedcontains solid megagametophytetis- additionallayer of elongate sclereidsin Cupres- sue in whichthere is no embryopreserved; there- sus funebrismarks the seed integumentat matu- fore, the innermostcells of this tissue are un- rity. A surfaceview of the seed of Pararaucaria known. No archegonia have been observed in shows that the sclereids are orientedin longitu- any ofthe seeds. dinal rows over most of the seed surfaceand not The elongate, slender micropylartube is ori- in isolated groups or bundles. If preservedas a ented toward the cone axis and tangentto it. compression fossil, the seed of Pararaucaria One vascular strandenters the seed fromthe dis- would probablyappear to have a striatedsurface tal portionof the ovuliferousscale (Fig. 6, 13). similarto thatreported for seeds of Elatides wil- There is a thinningof the stonylayer in th-eregion liamsoni by Harris (1943) fromthe Jurassicof of attachmentand a pad of thin-walledparen- Yorkshire,and Elatocladus ramonensisby Lorch chyma cells just outside the integumentswhich (1967) fromthe Jurassicof Israel. Calder (1953) referredto as a possible abscission Externalto the stonylayer are the possible re- zone (Fig. 13, arrow). Outside this zone is a mains of a fleshylayer of cells which appear group of small diametertracheids which usually crushed in most cases (Fig. 88). Cells in this have a lobed, rectangularconfiguration in cone regionwhen they are preservedare 20 ymin diam longitudinalsections (Fig. 13). and relativelythin-walled. Wieland (1935) describeda cone of Pararau- Seed wingsare small and measure a maximum caria patagonica (P13939) that contained two of 2 mm in length. They are composed of seeds per ovuliferousscale, and in this studyan- anastomosingrows of glandularhairs with patches other specimen (P13979) has also yielded two of thin-walledcells and many intercellularspaces seeds per scale (Fig. 10). Externallythese cones (Fig. 9). These hairs are continuouswith those appear identicalwith some of the largerPararau- on the upper surfaceof the ovuliferousscale. A caria specimens. Seed integuments,cone vascu- similartype of seed wing to that of Pararaucaria larization and other featuresof these cones are was foundonly in Abies grandis(Fig. 12) whose indistinguishablefrom other cones of this taxon, surfacereveals a seriesof anastomosingcells, some suggestingthat such variation occurred within that end in rounded tips such as those seen in the genus in low frequency. Mitra (1927) and Pararaucaria seed wings and on ovuliferousscale Wilde and Eames (1955) point out variationsin surfaces. Most of the other taxa examinedhave seed numberin- the genus Araucaria which has wingscomposed of 1-3 layersof elongatestraight one seed per scale in most cases but in rare in- walled cells, or cells with slightlywavy margins stances may have two to three seeds per scale. with no intercellularspaces or anastomoses. In cones of Pararaucariawith two seeds per scale, Seeds of Araucaria are typicallywingless. there is no massive interseminalridge as occurs The nucellus is preservedin most seeds as a in Pseudoaraucaria (Fliche, 1896; Alvin, 1953, thinlayer of crushedcells thatattaches only at the 1957a, b). seed chalaza. This tissueappears wavy in outline in mostseeds. Embryos-The majorityof seeds are sterile; The megasporemembrane is thin and appears however, where embryos are present,they are crushedwhen present. Remains of megagameto- exceptionallywell-preserved. The embryos of phyte cells are often present as a few rows of Pararaucaria patagonica are well-developed(Fig. slightlycompressed cells (Fig. 14, 15, 18, 19). 14-20). The shoot apex, ,hypocotyl, Cells are 60-90 ymin diam, containgranular ap- rootmeristem, and calyptroperiblemare all present pearingcell contents,and oftenspherical cellular indicatingthat embryosmay have been in the

Fig. 14-20. Pararaucaria patagonica embryos. 14. Longitudinalsection of telo-stageembryo. 031217 #1. X 28. 15. Oblique embryosection with cellular megagametophyte. 031217 #1. X 30. 16. Embryotissue with spherical cellular inclusions.031218 #2. X 300. 17. Transversesection of embryowith 8 cotyledons.031218 #4. X 20. 18. Transversesection of embryoat cotyledonarynode. 031218 #2. X 22. 19. Transversesection of embryoin hypocotylregion. 031217 #2. x 22. 20. Transversesection of embryoin calyptroperiblemor "root cap" region. 031218 #2. X 25. cal, calyptroperiblem;cot, ;h, hypocotyl;i, integument;m, megagametophyte;n, nucellus;ost, ovuliferous scale trace;rm, root meristem; sa, shoot apex; sc, sclerenchyma;w, wing. 740 AMERICAN JOURNAL OF BOTANY [Vol. 64 dormantstate when fossilized (Fig. 14). Some have been described in the hypocotylof Arau- cellular remains of the megagametophyteoccur caria mirabilis from this locality (Stockey, around the embryoproper withcrushed nucellar 1975a). tissuesurrounding them. There is no provascular tissue apparentin thissection, but it does appear DIsCUSSION-With the advent of more recent to be presentin transversesections of some coty- investigationsof livingand fossilconifers, and in ledons. Cellular detail of the tissue is particularcone vascularizationand resin canal well preserved. Delicate cell walls as well as cel- distribution(Miller, 1969, 1970, 1972, 1973, ular contentsand small sphericalstructures (5-6 1974a, b, 1976; Miller and Robison, 1975), it fLmdiam) like those in pithcells are present(Fig. is possible to compare more thoroughlythis fos- 16). The protodermespecially, coveringhypo- sil genus with those of both extant and extinct cotyl and cotyledons,shows excellent preserva- coniferfamilies. Historically,Pararaucaria pata- tion of cell walls and the small spherical struc- gonica has been placed in a number of tures (Fig. 16). These structuresmight have familiesby differentauthors. Wieland (1935) representeda numberof thingsin the livingstate: believed it to be intermediatebetween the Pina- proteinbodies, starch grains,oil globules, other ceae and the Araucariaceae on the basis of seed stored food material, condensed cytoplasm,or number, large expanded cone-scale complexes, most probablynuclear material. Their size range and cone vascularization. Calder (1953) placed and positionwithin the cells would seem to favor it in the Taxodiaceae based on a combinationof the latterview. Additionalsupport for thisinter- charactersincluding the large conspicuous bract pretationis their similarityand presence in a and ovuliferousscale, lateral seed attachment, number of differenttissues-megagametophyte, winged nature of the seed, and cotyledonnum- embryo,and pithparenchyma cells. ber. Archangelsky(1968) placed Pararaucaria The shoot apex is about 200 ,umin diameterat in the Cheirolepidaceae (Hirmer and H6rham- the point of attachmentof the cotyledonsand has mer, 1934) a familyof Mesozoic coniferscon- one prominentsurface layer of cells also withcel- tainingabout six genera. Wieland (1935) sug- lular contents. The hypocotyl extends for a gestedthe Cheirolepidaceaefor Pararaucaria due lengthof 1.8 mm below the shoot apex and coty- to the peculiar combinationof charactersof the ledonary node. The generativemeristem of the cone. Hirmerellamunsteri (Schenk) Jungcomb. root can be distinguishedin the fossil by the nov. (= Cheirolepidiummuensteri (Schimper) change in orientationof the cells fromhypocotyl Takhtajan) and Tomaxellia Archangelskycon- to calyptroperiblem(Fig. 14). The calyptro- tain two seeds per scale. Pararaucaria has one periblem or "root cap" (Buchholz and Old, or two seeds per scale, the usual numberbeing 1933) extends beneath the root meristemfor a one. Members of the Cheirolepidaceae, how- lengthof 0.9 mm (Fig. 14, 20). Also apparent ever, are characterizedby having prominently in the fossilembryos is the column or columellar lobed cone-scale complexes. Since most of the region that in living coniferembryos adds cells specimensof Pararaucaria studied thus far have to the "root cap" by periclinaldivisions (Allen, undergonesome weathering,the tips of the ovulif- 1947). erous scales or cuticle are not presentfor com- Figures 17-20 representa series of transverse parison. In cones where thereis a large portion sectionstaken through the embryo of Pararaucaria. of the ovuliferousscale presentthe scale appears Figure 20 representsa transversesection through striatedand unlobed (Fig. 2). Compressedcones the tip of the calyptroperiblemin which the cells of Tomaxellia have the same general dimensions can be seen convergingtoward a central point, as those of Pararaucaria, but shed their scales the column or columellarregion. Figure 19 is a and retained their seeds at maturitylike extant section throughthe embryohypocotyl, and at a araucarians (Archangelsky,1968). higherlevel (Fig. 18) throughthe cotyledonary Calder (1953) in a table of positive correla- node. The indicationof a three-partedsymmetry tionwith some familiesand generaof Coniferales, and the presenceof threedistinct lobes or cotyle- compared Pararaucaria to the extant Araucaria- donaryprimordia are seen in Fig. 18, an embryo ceae, Pinaceae, Taxodiaceae, and Cheirolepida- which had six cotyledons. Figure 17 shows an ceae. Many characterswere difficultto correlate embryowith eight cotyledons,probably the re- to any degreebecause of the typesof information sult of the dissectionof each of fourcotyledonary available due to differencesin preservationtype primordia. There are 6-8 cotyledons per em- among the fossilsand the currentstate of knowl- bryo, eight being the common number. This edge of livingconifers. Members of the Cheiro- cotyledonnumber corresponds to embryosin the lepidaceae, for example, are preserved as com- Pinaceae (2-15) and the Taxodiaceae (2-9) pressionswith cuticular remains and are difficult (Butts and Buchholz, 1940; Bierhorst, 1971). to compare in many cases with the petrifiedre- Araucarians commonlyhave 2-4 cotyledonsper mainsof Pararaucaria. embryo (Burlingame, 1915). No resin canals Externally,the cone resembles genera of the have been seen in embryotransverse sections as Taxodiaceae, in particularSciadopitys and Se- July, 1977] STOCKEY-PARARAUCARIA PATAGONICA 741

quoiadendron. The degree of fusionof the bract sus funebrisdescribed by Konar and Banerjee and ovuliferousscale is more pronouncedin these (1963) in numbers and appearance of sclero- genera which show prominentbracts (Hirmer, testal layers. The fossil Cunninghamiostrobus 1936). The Pinaceae, on the other hand, are hueberi (Taxodiaceae) was also described as usually characterizedby an inconspicuousbract having a multi-layeredseed integument(Miller, (Hirmer, 1936; Miller, 1976). The ovuliferous 1975). The holotype(USNM #31639) was re- scale of Pararaucaria is the dominantstructure examined in this study and revealed a similar withinthe cone-scale complex. This feature,un- structureto the integumentsof Pararaucaria in like the situationseen in araucarians,is similar longitudinalsection. The sclerotestacontains a to that in the Pinaceae and the Taxodiaceae. layer of radially elongate sclereids surrounding Eames (1913) points out that bract or scale a region of isodiametricsclereids. The presence dominanceis a characterthat varies in the Tax- of two radiallyelongate rows of sclereids,a fea- odiaceae, in particularin the genus A throtaxis ture which indicates a later developmentalstage Don. Within this genus, A. cupressoides Don in Cupressus and other genera, was observed in shows an ovuliferousscale larger than the bract, one seed. Cunninghamiostrobusseeds do not, A. laxifoliaHooker has a scale equal in size to however,show a ribbedintegument or prominent the bract, and A. selaginoides Don has a bract sclereidgroupings. largerthan the ovuliferousscale. Miller (1976) The general shape of the seed itselfis similar also points out that in the Pinaceae superficial to pinaceous types. The distal extentof the wing appearances of fossil cones are of limitedvalue is not known for certainbecause many cones of and can be highlymisleading. Pararaucaria have undergone some weathering; Romeroites, a genus of taxodiaceous cones however,the maximumseed wing lengthappears fromthe Neuquen provinceof Argentina(Speg- to have been approximately2 mm. The one azzini, 1924), is a structurallypreserved cone characterwhich Calder believed might indicate describedfrom a singlecone specimenand some affinitiesfor Pararaucaria outside the Taxodia- fragments.The dimensionsand externalappear- ceae is seed development. Taxodiaceous seeds ance are very similar to those of Pararaucaria are free throughouttheir developmentfrom the which promptedFlorin (1940, 1944) to suggest fertilescale except in the basal region (Pilger, that the two mightbe identical. Internal struc- 1926). Pinaceous seeds are not free duringde- ture reveals, however, many-seededovuliferous velopment,their wings being derivedfrom ovulif- scales, orthotropousseeds, and a bract and scale erous scale tissue. Most Pararaucaria seeds that are reportedlyfused for a greaterpart of studied by Calder (1953) and in this investiga- theirlength. tion are separated fromthe scale except at the Cone vascularizationinterpreted by Wieland as chalaza. The similarityof the seed wingsto the being like Pinus, and by Calder (1953) as being upper scale surface,however, and the attachment like the Pinaceae, Araucaria (section Bunya), of the wings in some cones to the ovuliferous and some Taxodiaceae was never really studied scale would indicate that developmentallythe in detail. In Pararaucaria, the ovuliferousscale wing probably arose from the ovuliferousscale and bracttraces are separateat theirorigins from tissue. Calder (1953) believed that if Pararau- the axis stele. The generalconfiguration is unlike caria could be shownto have pinaceous seed-wing thatof Pinus and certainPityostrobus but is simi- developmentthat it shouldbe placed withina new lar to Pseudoaraucaria and other genera of the family intermediatebetween the Pinaceae and Pinaceae. The ovuliferousscale trace has the theTaxodiaceae. abaxially concave configurationlike that of a Structureof the seed wingsis similarto thatof pinaceous cone (Miller, 1976, Fig. 1) and unlike pinaceous genera such as Abies. The anatomos- that of taxodiaceous or araucarian forms (Ra- ing stellate sclereidswhich Calder (1953) com- dais, 1894; Worsdell,1899; Aase, 1915; Hirmer, pares to the "cellules etoilees" of Abies nordman- 1936). The bract trace is stout unlike most niana described by Radais (1894) are here pinaceous genera, except Pseudoaraucaria and interpretedas glandular,hair-like trichomes simi- some Pinus species (Miller, 1976). It splits and lar to those found in Cedrus by Chowdhury becomes extensiveas in many cones of the Tax- (1961), which also occur on the surfacesof the odiaceae (Eames, 1913; Radais, 1894). ovuliferousscale and fromwhich the wings are Seed numbers are similar to the Araucaria- derived. They may have functionedin cone ceae. The Taxodiaceae usually have 3-5 seeds closure after pollination by the production of per scale, althoughas few as two and as manyas resinoussubstances as theydo in Cedrus. Of the nine seeds per scale have been reported (Bier- 20 taxa of pinaceous seed wings figuredby Tu- horst,1971). The extantgenera of the Pinaceae beuf (1892), only Pinus wallachiana A. B. Jack- are characterizedby two seeds per scale. son (= P. excelsa Wallich) and Cedrus libani A. Many-layeredseed integumentsare known to Richard showed cells of the seed wing that ap- occur in the Taxodiaceae and Cupressaceae. pear to anastomose and to contain some inter- Pararaucariashows some resemblanceto Cupres- cellular spaces. A similar structureoccurs in 742 AMERICAN JOURNAL OF BOTANY [Vol. 64

Abies grandisseed wings (Fig. 12). Seed wings canals associated with the sclerenchyma of of other species have cells withstraight or wavy Pararaucaria. Their peculiartriangular configura- marginsand no intercellularspaces. tion and persistencein the scale is unknownin The structureof the embryois similarto that other conifer genera. Calder (1953) suggests of otherliving conifers at the telo-stageperiod of that these sclerenchymastrands may have been development(Schopf, 1943). No leaf primordia associated with the separation of the scales at have been observed in shoot apices as occur in maturityand the liberation of seeds. Thus in Cedrus (Buchholz and Old, 1933). All the Pararaucariawe not only see evidenceof a mech- typical featuresof a coniferembryo at this de- anism for cone closure afterpollination by the velopmentalstage are present: shoot apex, coty- glandular hairs of the scale surface but also a ledons, root meristem,hypocotyl, and calyptro- possible mechanismof cone openingafter matura- periblem or "root cap." Cotyledon number is tion to effectseed release. Pararaucariaprobably similarto that in the Pinaceae and Taxodiaceae. retainedits scales and shed its seeds at maturity The most commonnumber of cotyledonsis eight like membersof the Pinaceae and Taxodiaceae. in Pararaucaria; although, six cotyledons are Evidence that the seeds were in fact released presentin some embryos. The transversesection fromthe scale can be seen directlyin the pres- in Fig. 18 is the cotyledonarynode of an em- ence of thick,woody bract and scale traces with- bryo withsix cotyledons. The threesegments or out abscission layers and an abscission layer at lobes of embryotissue representthe numberof the seed chalaza, and indirectlyby the absence cotyledonaryprimordia in Pararaucaria. Lobing of isolated cone scales at the Cerro Cuadrado at the cotyledonarynode is knownto indicatethe localities. numbersof cotyledonaryprimordia, for example Fossil ovulatecones of Pararaucariapatagonica in Larix (Schopf, 1943, Fig. 73, 77). Three or do not conformto any extinctor extant conifer four lobes are common in Pararaucaria. In genus but instead combine a numberof features Buchholz's (1919) studiesof pinaceous embryos fromfour or five familiesof conifers. The one- he found that several genera show a fusion of seeded conditionof araucariansis almostthe only cotyledonaryprimordia to give the numbers of featurelinking it with that group; Pararaucaria cotyledons seen in the mature state. Many representsa misnomersuggesting a relationship showed no cotyledonaryfusion and none showed thatprobably does not exist (Gothan, 1950). the splittingof cotyledonaryprimordia to give the The systematicposition of Pararaucaria would numbersof cotyledonsseen in the mature em- also appear to be more Pinaceae centeredthan bryo. In Pararaucaria,however, the threecotyle- has been thoughtby previousworkers. This idea donary lobes probably representthe number of corresponds partiallyto what Wieland (1935) cotyledonaryprimordia that, upon dichotomizing, originally suggested. Pinaceous characters in- resultedin the six cotyledonsseen in such em- clude vascularizationof the cone-scale complex, bryos. Thus Pararaucaria is differentthan Buch- seed wing features,cotyledon numbers, and sec- holz's pinaceous generain thisfeature. Cotyledon ondaryxylem pitting. Seed integumentsare tax- asymmetryobserved at the cotyledonarynode odiaceous and cupressaceous. Taxodiaceous in Pararaucaria (Fig. 18) is the common case charactersalso include the conspicuous, woody in embryosof the Pinaceae (Buchholz, 1919). bract and stronglydeveloped bract trace, cotyle- Polycotyledonyin Pararaucaria is noteworthy, don numbers,pith structure,and since secondaryxy- this conditionfor coniferembryos existed lem lackingresin canals. Pararaucaria is a petri- concomitant withthe dicotyledonouscondition in faction genus; therefore,comparisons with the Araucaria mirabilis (Stockey, 1975a). The sug- Mesozoic Cheirolepidaceae (Hirmerella and gestionthat polycotyledonyin conifersgave rise Tomaxellia) are limited. to the dicotyledonous condition (Buchholz, This study supports Calder's idea that seed 1919) will have to be re-examinedin fossilsfrom numberin fossil cones appears to have a limited sedimentsolder than the JurassicCerro Cuadrado diagnosticvalue and that of Miller (1976) that deposits. externalresemblances of fossil cones are often Of some interestare the two triangularshaped misleading. Takhtajan (1953) suggeststhat the strandsof sclerenchymaarising in the cortex of Taxodiaceae may have arisen from the earliest the cone axis of Pararaucaria thataccompany the primitivePinaceae. The intermediateposition of ovuliferousscale trace on its adaxial face into the Pararaucaria between the Taxodiaceae and the distal part of the scale. Miller (1970) reportsa Pinaceae may lend supportto this interpretation. dense tissue of sclereids,filling the gap between It may, however,suggest the opposite, i.e., the the tracesof the bractand scale and followingthe Pinaceae may have arisen from primitivetaxo- traces out into the cone-scale complex of Picea diaceous stock. It is the opinion of this writer diettertiana.Extending through this sclerenchyma that the genus Pararaucaria is sufficientlydiffer- are two resin canals. The number varies from ent in the combinationof charactersto warrant 2-13 in the genus Picea. There are no resin familystatus, and that furtherinvestigations of July, 1977] STOCKEY-PARARAUCARIA PATAGONICA 743

Jurassicage coniferswill providethe opportunity CHOWDHURY,C. R. 1961. The morphologyand em- of placing Pararaucaria in the properperspective bryologyof Cedrus deodara (Roxb.) Loud. Phyto- withreference to otherconifer families. morphology11: 283-304. DARROW,B. S. 1936. A fossilaraucarian embryo from The excellentsilica permineralizationof Par- the Cerro Cuadrado of . Bot. Gaz. 98: araucaria whichhas allowed developmentalinter- 328-337. pretationsof A. mirabiliscone structuresfrom the DOYLE, M. H., AND J. DOYLE. 1948. Pith structurein Cerro Cuadrado localities (Stockey, 1975b), and conifers. 1. Taxodiaceae. R. Irish Acad., Dublin, the large numbersof specimens available, have Proc. 52: 15-39. provided us with informationabout the repro- EAMES, A. J. 1913. The morphologyof Agathis aus- ductive strategiesof the : the retentionof tralis. Ann. Bot. 27: 191-204. scale, sheddingof seeds, possible mechanismfor FERUGLIO,E. 1949. Descripcion geol6gicade la Pata- gonia. 1. Buenos Aires. seed dispersal,and mechanismfor cone closure 1951. Piante del Mesozoico della Patagonia. after pollination. The polycotyledonouscondi- Pubbl. Ist geol. Univ. Torino. 1: 35-80. tion is seen to have existed in Pararaucaria dur- FLICHE, P. 1896. Itudes sur la flore fossile de 1'- ing the Jurassicand probablycame about by the Argonne (Albien-Cenomanien). Bull. Soc. Sci. dissectionof cotyledonaryprimordia. Preserva- Nancy. 14: 114-306. tion of the delicate embryotissues, so rare in the FLORIN, R. 1940. The Tertiaryfossil conifers of South and theirphytogeographical significance, with fossil record, has allowed direct comparison of a reviewof the fossil conifersof southernlands. the telo-stageembryo of Pararaucaria to those of K. Sven. Vetenskapsakad.Acad. Handl. Stockholm. living conifers at a comparable developmental III, 19: 1-107. stage. 1944. Die Koniferen des Oberkarbons und des UnterenPerms. Heft 7. PalaeontographicaB. 85: 457-654. LITERATURE CITED GOTHAN,W. 1950. 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