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Aspects of Cone Morphology and Development in Podocarpaceae (Coniferales)

Author(s): P. B. Tomlinson
Source: International Journal of Plant Sciences, Vol. 153, No. 4 (Dec., 1992), pp. 572-588
Published by: The University of Chicago Press
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Int. J. Plant Sci. 153(4):572-588. 1992.
? 1992 by The University of Chicago.All rightsreserved.
1058-5893/92/5304-0007$02.00

ASPECTS ANDDEVELOPMENT
OFCONEMORPHOLOGY
IN PODOCARPACEAE
(CONIFERALES)l
P. B. TOMLINSON
HarvardForest, HarvardUniversity, Petersham,Massachusetts01366

Ovulate cones in most Podocarpaceaeconsist of one or more fertile units, each composed of a fertile
bractsubtendingan axillaryepimatiumthat supportsa single adaxialinvertedovule. Cones may consist
of numerousunits, up to ca. 20 in Microcachrys,but show progressivereductionin differenttaxa to the
ultimatecondition in which there is only a singlepseudoterminalovular unit. In the developmentof the
ovular complex the solitaryovule arises from the surfaceof the preexistingepimatium.The sequenceof
parts is acropetal,rather than basipetal as previously reported.The consistency of the developmental
process supportsthe hypothesis that the function of the epimatium is to produce an inverted ovule,
essentialfor pollen scavengingvia an extendedpollinationdrop. Cone structureand position in relation
to shoot construction,phenologyof cone development,and correlationbetweenthe timingofdevelopment
in cones and parentshoots are all shown to be interrelated.

Introduction late in seed maturation(Tomlinson et al. 1989).


The aril then could be either the precursorto the
Many Podocarpaceae (podocarps) exhibit an
than its reducedvestige, or an
unusual method of pollen receptioninvolving an epimatium, rather
extended pollination drop that could scavenge entirely independent structure. Saxegothaea
pollen in the vicinity of the micropyle (Tomlin- seems isolated and highly derivedwithin the fam-
ily. It has an epimatium but lacks a pollination
son 1991; Tomlinson et al. 1991). This process on the cone scale,
of pollen scavenging is correlated with an in- drop since pollen germinates
verted ovule that also may permit saccate pollen outside the micropyle so that male gametes are
delivered by extended siphonogamy to the dis-
to float upwardinto the micropyleand the pollen tinctive extruded nucellus
chamber (Doyle 1945). Ovule inversion is also (Noren 1908; Doyle
and O'Leary 1935).
stronglycorrelatedwith the presenceof an ovule- Much of this newer interpretationdepends on
supportingstructure,epimatium, that is distinc- the
assumption that the epimatium in different
tive to, but not ubiquitous in, the family since it taxa
representsthe same structure.In the present
doesnot occurin Microstrobos andPhyllocladus. article evidence in support of this homology is
It was suggestedthat the correlationis functional derived from
since it is the epimatium that provides the de- a study of the ontogenyof the ovule-
supporting complex in Podocarpaceae, where-
velopmental mechanism for inversion of an oth-
upon it can be shown that the ovule is an
erwise orthotropousovule. The adaptive driving appendageof the prior epimatium andclearly that con-
force for these unusualfeaturesof podocarpsmay fusion between in podocarpsand ovu-
be the trend in the family for reductionof ovules liferous scale inepimatiumother conifers can easily lead to
in each cone. This in turnis relatedto the frequent
the idea that the two are homologous.
presence of large, heavy seeds with associated
colored and often fleshy structuresthat serve as
attractants for animal dispersal agents, mainly Materialandmethods
birds. In many podocarps, cones are so reduced Material was obtained for 11 species in seven
that they may contain only a single ovule. This genera that show early stages of cone develop-
biological perspective on cone morphology in- ment (table 1). More extended comparison was
dicates a modificationof the usual interpretation possible by single collections of additional taxa
of the epimatium, which, following the work of (table 2). Only two of these taxa, one with lateral
Florin (1954) is always interpreted as the ho- cones (Podocarpuselatus; figs. 29-40) and one
mologue of the ovuliferousscale of otherconifers, with terminal cones (Dacrycarpusdacrydioides;
e.g., Pinaceae.In the newerinterpretationthe epi- figs.41-51) areheredescribedin detail,with some
matium is considered to be an entirely novel documentation of significantstages added to il-
structureand the cone ancestrally simple. This lustrate the range of diversity in other species
would place the two anomalous members of the (figs. 52-64). Materialwas obtained during field
family, Microstrobosand Phyllocladus,which study of populations in which pollination mech-
have erect ovules and lack an epimatium in an anisms were initially observed. However, in or-
ancestralposition. Phyllocladusdevelops an aril der to obtain a rangeof developmental stages, an
understandingof shoot and cone phenology was
IReprintsavailablefrom the author. obtained by repeated visits to several localities
ManuscriptreceivedJune 1992; revisedmanuscriptreceived over a period (September 1989-January 1990).
July 1992. This fieldwork was carried out mainly in New
572

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TOMLINSON-PODOCARP CONE DEVELOPMENT 573

Zealandbut with additional cones supplied from


Tasmania and New South Wales (see Acknowl-
edgments). Developmental stages of taxa other u
- - - - - - - - - - -

than those described in detail were not always


complete but are sufficientto show a patternuni-
form for the family.
Cone primordiawere fixed in FAA in the field
or subsequentlyin the laboratoryand dissected
undera Wild M-5 stereomicroscope.For prelim-
inarysurveysof cone morphologydissected spec-
imens were stained in 1%Acid Fuchsin in 95%
ethanol and examined either under a stereomi- S 0 cl
croscope or with epi-illumination dipping cones
as in the techniques of Posluszny et al. (1980).
Material for photographic documentation was
criticalpoint dried and examined underscanning
electronmicroscopy(SEM)either at the Museum
of ComparativeZoology (AMR 1000), Harvard
University, or at the Departmentof Botany, Uni-
z Q~z Q
versity of Massachusetts(JEOL5200).

Results
CONE POSITION AND PHENOLOGY
A basic comparison can be made between a
cone and a vegetative shoot (figs. 1, 2). Vegetative
shoots show seasonal increments of growth and E~~~~~~ 3o32|g3
usuallyhave spirallyarrangedleaves;lateralbuds
are discontinuously distributed along the shoot.
A branchshoot alwaysbeginswith a pairof lateral
prophylls (fig. 2). A cone differs from this in its
continuous production of axillary ovuliferous
complexesand its determinatebut not necessarily : : : : : t

continuous development (figs. 2, 12).


Cones in podocarps may be either terminal or
lateral,and thereis some correlationbetweenthis XZ <3 3a
position and leaf type. Terminal cones occur in
all genera with scalelike, awl-shaped, or bilater-
ally flattenedadult leaves, as representedby Hal-
ocarpus, Dacrydium, and Falcatifolium, respec-
tively. Such taxa lack bud scales and pronounced
shoot articulations and produce vegetative
branches of up to two orders within a seasonal
growingcycle. Sucha phenologyand construction
precludes the development of short specialized
laterals (figs. 3, 5, 10, 11). In taxa with terminal
cones the position of fertileaxes is not predictable
and sampling for early stages may be fairly ran-
dom. However, in Lepidothamnus laxifolius,
cones occur on the second-orderaxes of the pre-
vious year's shoot increment and can be located
with some precision. Fertile axes, i.e., those with
young cones, can sometimes be recognized by
theircharacteristicswollenshapewell beforecone
expansion,e.g., Dacrycarpusdacrydioides.In this
species cone primordiacan be recognizedas early
as the March (late summer)prior to cone expan-
sion in September (early spring). In contrast, in
Dacrydium cupressinum,cone initiation occurs
only a month or so before pollination in Decem-

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574 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Table2
FLUID PRESERVED MATERIAL OF OVULATE AND SEED CONES USED IN PREPARING
FIGURES 1-28

Species Location Collector


Afrocarpusfalcatus............ Kenya JEB
Dacrycarpusdacrydioides...... New Zealand ECK and PBT
Dacrydiumcupressinum....... New Zealand PBT
Decussocarpuscomptonii ...... New Caledonia J-MV and PBT
Falcatifoliumtaxoides ......... New Caledonia J-MV and PBT
Halocarpuskirkii ............. New Zealand JAR and PBT
Lagarostroboscolensoi ........ New Zealand JAR and PBT
Lagarostrobosfranklinii....... Tasmania AS and PBT
Lepidothamnuslaxifolius ...... New Zealand JAR and PBT
Microcachrystetragona........ Tasmania PBT
Microstrobosnipophyllus....... Tasmania PBT
Nagaei nagi ................ Japan NK
Parasitaxusustus ............. New Caledonia J-MV and PBT
Phyllocladustrichomanoides... New Zealand PBT
Prumnopitysferruginea........ New Zealand EKCand PBT
Prumnopitystaxifolia ......... New Zealand JAR and PBT
Podocarpuselatus ............. New South Wales CJQ
Podocarpusnivalis ............ New Zealand PBT
Saxegothaeaconspicua ........ Cult. Ireland JW and PBT

Note. Nomenclature is after DeLaubenfels(1972, 1988) and Page (1989,


1990). The numberof collections for each species varies widely, dependenton
accessibility.The initialsof the collectorsareas follows:JEB= John E. Braggins;
EKC = Ewen K. Cameron; PBT = P. B. Tomlinson; J-MV = Jean-Marie Veillon;
JAR = Jack A. Rattenbury; AS = Alison Shapcott; NK = N. Kawakubo; CJQ
= Chris J. Quinn; and JW = Jim White.

ber and can be recognized initially by the up- branches,within the terminal bud shortly before
turning of the otherwise pendulous shoot apex, the bud goes dormant. Since apices of vegetative
coincidentwith generalregrowthof shoots. In the and reproductive meristems are initially identi-
firstexample, cones exist in a dormant condition cal, the actual time of induction of cones is not
for an extended winter period, but not in the certain. Cones are usually borne at the base of
second. It is not the intention here to describe each new shoot increment and are subtended by
the phenologyof each speciesin detail, but it must scale, transitional, or basal foliage leaves. Cones
be emphasized that cone induction is not exter- may overwinter (i.e., undergo rest), but syllepsis
nally visible and may predatecone expansion by best describestheir continued development since
several months. In view of the wide variation in they initiate most appendagesand expand con-
latitudeand altitudeat which some species occur, temporaneouswith the extension of the terminal
precise statements should not be generalizedfor bud that forms the current-yearshoot. As in syl-
all populations. Representative data for taxa in leptic vegetative branches there is a shorter or
the natural areas are cited under "Phenology" longer hypopodium (the peduncle of the cone)
table 1. below the first pair of leaves (prophylls),which
Lateralcones occur in genera with needle-like may or may not be fertile, i.e., subtend ovules.
(e.g., Podocarpus),linear (e.g., Prumnopitys)or Ovule initiation occurs at or shortly after expan-
broadly ovate leaves (e.g., Nageia). The time of sion of the parent vegetative shoot from within
cone expansion varies in differentgenera in re- the enveloping scales of the terminal bud. No
lation to shoot extension, and the terms "prolep- other podocarp shows this sylleptic condition.
sis" and "syllepsis"may be applied.Lateralcones Proleptic development of cones occurs in
that areprolepticin originmay still undergosome Prumnopitys(figs. 10, 11) since lateral buds that
development immediately after initiation. Since are initiated on the current shoot remain either
relatively few species have been examined in the unextended(Prumnopitystaxifolia) or grow only
field, the correlations between phenology and slowly (Prumnopitysferruginea) during the dor-
morphology are tentative but are supported by mant season. In P. ferruginea, cones are located
examination of specimens in the Harvard Uni- at some of the basal nodes of the previous year's
versity Herbaria. increment (fig. 11) and grow slowly in winter,
Podocarpus(sensu stricto Page 1990) is very adding new scale leaves so that they become pro-
uniform and the small number of cone append- gressively more conspicuous as grublike struc-
ages is correlatedwith sylleptic development (fig. tures and easily distinguishable from dormant
5). Lateral cones are initiated, as are vegetative vegetative buds. However, ovule initiation does

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TOMLINSON-PODOCARP CONE DEVELOPMENT 575

~~IIii~~ prophyll 7

\ ? X4 3

S vegetative shoot '

I / (

~~~~~~~~prophyll

/lK> ( foliage leaf


K) scale, or sterile bract

erminal cone fertile bract

~3epimatium
with
inverted ovules

erect ovules
0 3 branch or parent axis
cone axis

Figs.1-4 Shoot morphologyin Podocarpaceae.Fig. 1, Diagramof vegetativeshoot with needle-likefoliage leaves, terminal
restingbud, rhythmicgrowth,and diffuseproductionof lateralbuds. Fig. 2, Diagramof lateralshoot with basal prophyllpair,
spiral(2/5) phyllotaxis,and axillarybudsof next branchorder,eachwith prophyllpair.Fig. 3, Diagramof shoot with overlapping
scale foliage, continuousgrowth,and cones terminalon higherorderaxes. Fig. 4, Key to symbols used in figs. 5-28.

not occur until shortly before cone extension in are linear, not scalelike, and yet it usually has
late spring(table 1). Such cones are thereforesub- terminal cones. Detailed phenological informa-
tendedby an extendedseriesof overlappingscales, tion of cone induction is not available. Phyllo-
produced in winter, which contrast with the few cladus shows extreme syllepsis. Phyllocladesde-
reflexedbractsdeveloped below the cone proper. velop just prior to the flushing cycle since the
Prumnopitys taxifolia differs in that the cones overwintering apex is naked but enveloped by
usually occur distally on the current-yearshoot bud-scales produced at the end of the previous
and produce relatively few basal scales (fig. 10). flush. Phyllocladesare neoformed, and cones are
The cone axis also extends at pollination and is initiated on higher order axes, occurring either
much longer, with numerous fertile bracts (up to on the base or margin of the flattened branches
12). At pollination these whitish candle-likeerect or on the margins of ultimate units. This genus
cones are very characteristic.Other podocarps is thereforeunusual in its very short cone cycle.
with lateral proleptic cones include Afrocarpus,
Nageia, and Sundacarpus,but these have not been CONEMORPHOLOGY
studied in detail. Cone structure is determined by, or at least
Saxegothaea is exceptional in that its leaves correlatedwith, its position, phenology, and, to

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576 INTERNATIONAL JOURNAL OF PLANT SCIENCES

PODOCARPUS SPP 0
prophyll epimatium ,
/i
fertile
bract )oe xi
he + 0 vule t

*leaf Podocarpus nivalis

fertile bract

prophyll1 I

Podocarpus t)g

Podocarpus elatus
Figs.5-9 Podocarpus species, with needle leaves and cones developed by syllepsis (i.e., contemporaneous with shoot extension).
Fig. S, Diagram of developing shoot with cones situated basally and functioning immediately. Figs. 6, 7, Cone morphology in
species represented by P. nivalis, the prophyll pair functioning as potential fertile bracts, with either one (fig. 6) or two (fig. 7)
fertile bracts; additional sterile bracts may occur (dotted outline in fig. 7). Figs. 8, 9, Cone morphology in species represented
by P. elatus with prophylls sterile, fertile bracts corresponding to second pair of leaves, and cones with either one (fig. 8) or
two (fig. 9) ovules. Dotted outline represents additional sterile bracts that may be present; "leaf" subtending appendage,
which may be an inner bud scale, a transitional leaf, or a foliage leaf.

a lesser extent, by the phyllotaxis of the shoot. In Correlationsalso occur with the timing of de-
Microcachrys,Nageia, and Decussocarpus,phyl- velopmental events in the cone in relation to the
lotaxisis decussate;the arrangementof cone scales phenology of the parentvegetative shoot. This is
is also decussatein the lattertwo genera(figs. 15, most distinctive in Podocarpus and is a conse-
28), but the fertile bracts are whorled in Micro- quence of sylleptic cone development (fig. 5). In
cachrys,with four units in each series (fig. 16). In many Podocarpus species, represented here by
Podocarpus,cone scales are also decussate (figs. Podocarpus nivalis (figs. 6, 7), there can be one
6-9), relatedto their syllepticorigin,with the first or two pairs of bracts, with either one (fig. 6) or
paircorrespondingto prophylls.Occasionalcones two bracts (fig. 7) fertile. These fertile bracts are
with decussatephyllotaxisoccur in taxa that oth- in the lateral (prophyllar)position. In cones in
erwise have a spiral arrangement(e.g., Lepido- which both prophylls function as fertile bracts
thamnus). (fig. 7), there is commonly a second pair of sterile
In all other genera cone bracts are spirally ar- bractsas the ultimate appendagesof the cone and
ranged (figs. 12-14; 17-19; 20-27), and the ar- in the dorsiventralposition. In other Podocarpus
rangementmay be directly comparableto a veg- species, represented here by Podocarpus elatus
etative shoot (fig. 2). In the cone diagrams (figs.8, 9), theremay be up to threepairsof bracts
representingspiral phyllotaxis, a consistent 2/5 in a decussate arrangement.The lower pair are
(2 + 3) arrangementis used, althoughthis is not alwayssterileand correspondto lateralprophylls,
necessarily so in actual cones; those with a few the second pair (in the dorsiventral plane) may
ovules are frequentlyirregular,with upper scales either both be fertile-and then sometimes with
displaced from the normal Fibonacci sequence. a final pair of distal, sterile reduced bracts (fig.
In shoots that have terminal cones (e.g., fig. 3) 9)-or more usually, only one of the second pair
the arrangementof bracts is normally consistent of bracts is fertile, and then almost always in the
with that of the foliageleaves immediatelybelow, adaxialposition (fig. 8), usually with the opposed
even thoughleaf structuremay changein the tran- abaxial bract present but not always. The most
sition from the vegetative to the reproductive common arrangementin P. elatus includes two
condition. lateral prophylls and a second pair of inflated

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TOMLINSON-PODOCARP CONE DEVELOPMENT 577

prophyll It
lateral cone

Prumnopitystaxifolia
,, II

Prumnopitys Prumnopitys
taxifolia ferruginea

~~~~~~~~~~~~~~~~~~~ i/

(V&-:fr ,/i j Prumnopitysferruginea

Afrocarpusfalcatus

Nageia nagi
Figs.10-15 Shoot and cone morphologyin Podocarpaceaewith lateralcones that develop by prolepsis.Figs. 10-13, Prum-
nopitysspp. Fig. 10, Shoot in P. taxifolia with cones appearingdiffuselythroughoutprevious increment.Fig. 11, Shoot in P.
ferrugineawith cones restrictedto base of previous increment.Fig. 12, Diagramof cone in P. taxifolia with numerousfertile
bractsand few basal scales. Fig. 13, Diagramof cone in P. ferrugineawith one (occasionallytwo) fertilebractsand extensive
series of basal scales. Fig. 14, Afrocarpusfalcatus,diagramof lateralcone with one or two fertilebractsand basal sterile scales.
Fig. 15, Nageia nagi, diagramof lateralcone with decussatephyllotaxis,single fertilebract,and cone axis with distal reduced
sterile bracts.

bracts at right angles, only the adaxial one being (figs. 10-13), the cone is always more elaborate
fertile (fig. 40). In all cones, the cone apex itself than in Podocarpusin terms of the largernumber
is consumed in the formation of the ultimate ap- of appendages.There is always a lateral pair of
pendages. prophylls(correspondingto those of a vegetative
Where lateralcones are producedby prolepsis branch) and a longer or shorter series of sterile

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578 INTERNATIONAL JOURNAL OF PLANT SCIENCES

(;t 2 t X ? + D X f2 Va)

Saxegothaea conspicua

Microcachrystetragona 1

18~ ~~ ~~~~~~~~(9

Microstrobosnipophyllus

Phyllocladus trichomanoides
Figs.16-19 Diagrams of cone morphologyin taxa with evident cones and numerousfertile bracts. Fig. 16, Microcachrys
tetragona,cones terminalwith basal sterilebractscontinuingdecussatearrangementof vegetativeshoot (e.g., a, a; b, b), fertile
bractsin whorlsof four,with membersof successivewhorlsalternating(1 1, 1, 1;2, 2, 2, 2, etc.). Fig. 17, Saxegothaeaconspicua
with terminal cones and numerousdistal sterile bracts. Fig. 18, Phyllocladustrichomanoides,cones lateral on phylloclades,
ovules erect with later-developingaril, no epimatium(cf. Tomlinson et al. 1989). Fig. 18, Microstrobosnipophyllus,terminal
cones with erect ovules and no epimatiumor aril.

scales, whose number seems primarilyto be de- taxon (figs. 16-28). Microcachrysmay have up
termined by the period that elapses before the to five whorls of fertile bracts, each with four
cone becomes dormant. Prumnopitysferruginea bractsper whorl, to a total of 20 ovules. The cone
is exceptionalbecauseof its continuedslow growth continues with usually a terminalwhorl of sterile
throughwinter while the parentaxis is dormant. bracts(fig. 16). This seems to be the largestnum-
Prumnopitystaxifoliaultimatelyhas a longercone ber of ovules per cone in the family. Saxegothaea
axis, since in its final phase of extension inter- (fig. 17) and Microstrobos(fig. 19) are also cone-
nodes are elongated, and there can be up to 12 like and with sterile ultimate scales.
fertile bracts(fig. 12), contrastingwith the one or The very distinct cone of Phyllocladusis anom-
two fertile bractsof P. ferruginea(fig. 13). Cones alous because of its extreme sylleptic origin. It,
in Afrocarpus(fig. 14), Nageia (fig. 15), and Sun- and the supportingphylloclade, are totally neo-
dacarpus(not illustrated,but similar to Afrocar- formed during extension growth of the current
pus) also include a series of sterile bracts above season shoot. The most frequent condition in
the prophylls,with one or two distal fertilebracts. Phyllocladus trichomanoidesincludes few or no
In Nageia there are usually additional distal re- basal sterile scales and about six fertile scales (fig.
duced sterile bract pairs (fig. 15). 18). However, the arrangementof parts is rather
In species with terminal cones the number of irregularin cones of this genus.
fertile bractsvaries, even within a single species, Most genera(figs. 20-27) have cones with spi-
but the rangeis limited and characteristicfor each rally arrangedbracts and can be seen as forming

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TOMLINSON-PODOCARP CONE DEVELOPMENT 579

Lagarostrobos franklinli Halocarpus kirkii

Lagarostrobos colensoi

Lepidothamnuslaxifolius

(23)t +

Dacrycarpusdacrydioides

Parasitaxusustus

Z/ 0\Dacrydium
X cupressinum

< cSS~~~~~( (I' d (VI''

Falcatifoliumtaxoides Decussocarpus comptonif

Figs.20-28 Diagramsof terminalcones in Podocarpaceae,mostly with scalelikefoliage(cf. fig. 3); cones erectin all examples
exceptfig.20. Fig. 20, Lagarostrobosfranklinii, cones pendulouswith extendedaxis;severalfertilebracts.Fig. 21, Lagarostrobos
colensoi cone with two to three fertile bracts;distal bracts sterile. Fig. 22, Halocarpuskirkii, cone with three to four fertile
bracts;distalbractssterile.Fig. 23, Dacrycarpusdacrydioides,cone with one or two fertilebracts,with late-developingreceptacle
(r);no distal sterilebracts(cf. fig. 46). Fig. 24, Lepidothamnuslaxifolius,cone with singlefertilebract;distal fertilebractalways
opposed to a sterile bract facing the epimatium (cf. fig. 59). Fig. 25, Parasitaxusustus,cone with single fertile bract. Fig. 26,
Dacrydiumcupressinum,cone with single fertile bract. Fig. 27, Falcatifoliumtaxoides, cone with single fertile bract. Fig. 28,
Decussocarpuscomptonii,cone with singlefertilebract;phyllotaxisis decussate.In figs. 25-28, thereare no distal sterilebracts;
the solitaryfertilecomplex may then appearterminal(e.g., fig. 28).

a series in which ovule number is progressively the longest intemodes; it is exceptional in this
reducedand cone structureprogressivelysimpli- group in its pendulous cones. Halocarpus kirkii
fied. Cones are more or less compact, and there has fewer fertile bracts (usuallythree to five) and
is usually a series of basal sterile bracts transi- a condensed axis (fig. 21). Lagarostroboscolensoi
tional from the subtending foliage leaves, al- contrastswith L.franklinii in its erect, somewhat
though in some taxa the transitionis abrupt(e.g., condensed cone axis and few (two to three)fertile
Dacrycarpus,fig.44). Lagarostrobosfranklinii has bracts (fig. 22). All these taxa have the cone dis-
the largest number of fertile bracts (fig. 20) and tally continuous into a series (two to three) of

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580 INTERNATIONAL JOURNAL OF PLANT SCIENCES

reduced,sterilebractsthat may form a cap to the the inception of irregularshallow lobes (figs. 35-
cone. In D. dacrydioidesthere is only one, less 37). In furtherdevelopment the common base of
commonly two, fertile bracts, and the cone is epimatium and bract begins to extend (fig. 37),
distinguishedby the long interval between bract the integument becomes more pronounced (figs.
initiation and final cone maturation, to be de- 36, 37), and the abaxial surfaceof the epimatium
scribed later (table 1). All other taxa illustrated extends and forces the ovule into an increasingly
(figs. 25-28) normallyhave only one fertilebract. inverted position (fig. 37). The distal (adaxial)
There may be sterile reduced bracts above this marginof the epimatium continues to grow, pro-
as in Lepidothamnus(fig. 24). Otherwisethe sol- gressivelyenclosingthe ovule (fig.38). Laterstages
itary ovule is pseudoterminal.In Lepidothamnus show a markedextensionof the epimatium,which
the regularphyllotaxis of distal bracts is some- soon exceeds the limits of the subtendingbract,
what distortedto producea sterilebractopposite the enclosure of the ovule, so that the nucellus is
the fertile one, an important component of the obscured, by the enlargement, both axially and
pollinatingmechanism. In Decussocarpuscomp- radially of the common base of the epimatium
tonii the cones are usually terminal,but if lateral and bract (fig. 39). At the time of pollination the
the basal pair of scales is in a prophyllarposition upperbractsmuch exceed the prophyllsand show
(dotted outline in fig. 28). The reduction series the enlargementthat presagestheir swollen con-
appearsto culminate in the taxa with pseudoter- dition at seed maturity. The epimatium exceeds
minal ovules, Acmopyle(not illustrated),Parasi- its subtendingbract, its apex is pointed (fig. 40),
taxus (fig. 25), Dacrydium (fig. 26) and Falcati- and the integument is completely enclosed, ex-
folium (fig. 27). The best candidatefor a terminal cept for the protrudingmouth of the micropyle
ovule complex is D. comptonii,but developmen- (figs. 39, 40).
tal stages have not been observed.
DACRYCARPUS DACRYDIOIDES (FIGS. 41-
CONE DEVELOPMENT
51). This species is distinguished by the bi-
modal sequenceof cone development.Earlystages
PODOCARPUS
ELATUS
(FIGS.29-40). Cones are of cone initiation up to the formation of the two
initiatedin the mannerof axillaryvegetativebuds to three robust bracts, can be found as early as
in association with lower leaves of each renewal March (late summer). The cone remains in this
shoot (fig. 5). The precise time of initiation is not condition until September,when epimatium and
known since it occurs within the restingterminal ovule initiation and bract extension begin, pro-
bud at the end of a previous unit of shoot exten- ceeding within 3-4 wk to cone maturationas far
sion. Earlystages of vegetative and reproductive as the stage of pollination. Figures 41-44 show
buds seem identical, but the two become distin- the transition from vegetative to reproductive
guishable after the development of the ultimate apices and the initiation of bracts;figures45-47
(secondor third)pair of appendages.These stages show the entirecone duringepimatiumand ovule
occur as the parent vegetative axis begins to ex- development, while figures48-51 show stages in
tend following bud burst. Initially, the prophylls the initiation of the ovule.
arewell advancedin development and exceed the Vegetative shoots have a pronounced dome-
second pair,in which one or both bractsarefertile shaped apex above the insertion of the youngest
(figs. 8, 9). In figures30-40, the development of visible leaf primordia (figs. 41, 42). The size of
only one fertile complex is followed; the facing the apex and phyllotaxis are determined by the
bract, either sterile or fertile, is removed. The vigor of the shoot; higherorderaxes on any shoot
epimatium is initiated in the axil of the fertile complex are always smallest. Reproductive api-
bract as a narrowelongated mound of tissue (fig. ces can most easily be identified,upon dissection,
30) that enlargesin proportionto the increasein by the two to three bract primordia that intrin-
size of its subtending bract but becoming nar- sically consume the apex (fig. 43). These bracts
rowed at the base (fig. 31). The apex of the bract proceed to a stage when they are short but thick-
usually becomes hooded and lobed, overarching ened radiallyand contrast with the primordiaof
the epimatium (figs.32-34). The epimatium may the foliage leaves immediately below (fig. 44). In
at firstappearconcave or irregularlylobed, seem- this condition the cones overwinter with a rela-
ingly the result of the pressureof facing append- tively inactive period of about 5 mo. Renewed
ages. First evidence for the development of the developmentin Augustis indicatedby intercalary
ovule is the appearanceofa centralshallowmound extension of the bract bases and the initiation-
on its adaxial side (figs. 32, 33). The integument above the axil of one of them (sometimes two)-
becomes differentiatedfrom the nucellus(figs.34- of the epimatium as a low mound of tissue (fig.
36) in association with the widening of the epi- 45). There is rapid extension of the bracts (fig.
matium, which also becomes thickened radially, 46) mainly by intercalarygrowthso that the ovu-
i.e., in the adaxial-abaxial plane. At this stage lar complex is carried up on the adaxial face of
also, the outermarginof the epimatiummay show the bract(fig. 47). Examinationof individual fer-

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a29 313
30

'4~~~~~~~~~~~~~~~~~~~~~~~~~~~~

35~~~~~ b~3

and epimatium all discrete. Fig. 37, Wideningand deepeningof nucellus, integument,and epimatium. Fig. 38, Epimatium
beginning to invert the ovule; integumentenveloping nucellus. Fig. 39, Ovule inventedand enclosed by epimatium; only
micropylarorifice protruding.Fig. 40, Maturecone at about stage of pollination,subtendedby a foliage leaf. b = bract;br =
bract removed;e = epimatium;f = foliage leaf;ft = foliage leaf removed;i = integument;m = micropyle;n = nucellus;o =
ovule; p = prophyll;r = receptacle.Bars = 200 ,umin figs. 29-38; 1 mm in figs. 39, 40.

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K~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~k
.48..

12
J.I
A#.~~~~~~~~~~~~~~~~~~; -A
L~~~~~~~~~~~~~~~~~

42~~~4
4ES ~~~~~

Figs.41-S1 Dacrycarpus dacrydioides, conedevelopment(cf. fig.23). Fig.41, Vegetativeshootapexfromthe side, apical


dome exceedingyoungest leaf primordia.Fig. 42, Vegetativeshoot apex from above; phyllotaxisapproximately3 + 5. Fig.
43, Young cone from above, with primordiaof three bractscontinuingthe phyllotaxisof the earhiervegetative shoot; apical
dome consumed. Fig. 44, Young cone in overwinteringcondition with threebractsclearlycontrastingwith older primordiaof
vegetativeleaves. Figs. 45-47, Whole cones from the side. Fig. 45, With one bractremoved,epimatiumvisible in axil of fertile
bract. Fig. 46, Oldercone from side to show bractswith disjunctmeristematicbase (the futurereceptacleof the maturecone);
bract tips almost mature.Fig. 47, Cone with two bracts,one removed;immatureovule inverted, surroundedby epimatium,
the micropylarorifice protruding.Figs. 48-51, Single ovular complex exposed by removal of facing bracts. Fig. 48, Early
initiationof epimatium,from adaxial(inner)surfaceof bract.Fig.49, Laterstagewith epimatiumlobed showingthe impression
of the two facingbracts.Fig. 50, Epimatiumwith youngovule; nucellusand integumentwell differentiated.Fig. 51, Epimatium
beginningto overarchthe ovule; bractbase beginningto extend, providingspace for the enlargedovule (cf. fig. 47). Labeling
as in figs. 29-40. Bars = 100 Mmin figs. 41-43; 200 ,umin figs. 44-46 and 48-51; 500 ,umin fig. 47.

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TOMLINSON-PODOCARP CONE DEVELOPMENT 583

tile complexes shows the inception of the epi- tercalaryextension of the bases of the bracts ex-
matium on the adaxial face of the bract as a low tends the whole unit on a common axis (fig. 59).
protuberance(fig.48). This enlargesand is carried The seed remains naked and erect at maturity,
up by the expansion and extension of the bract with the epimatium forming a short lobed collar
base so that it soon appearsto be situated on the at its base. Subtendingsterilebractsbecome fleshy.
adaxial face of the bract (fig. 49). It may appear In P. taxifolia, the epimatium is an axillary
lobed because of the pressureof the facing sterile structure(fig. 60). This is a view of the abaxial
bracts(fig. 50). Integumentdifferentiationdelim- side with the subtending bract removed. In this
its the nucellus.This is clearlywithin the confines species there is little intercalaryextension of the
of the epimatium since the prior lobing does not complex so that bractand epimatium remaindis-
significantlyinfluence the outline of the integu- crete. The ovule is initiated on the adaxial side
ment (fig. 50). With furtheruniform enlargement of the bract in the usual way (fig. 61), the epi-
of the complex, nucellus (n), integument (i), epi- matium much exceeding the young ovule, which
matium (e), and bract (b) are discretelyseparated is consequentlyinverted from the start.The bract
(fig. 51). Later expansion of the epimatium in- plays no part in dispersal, the fleshy layer of the
volves the enclosure and inversion of the ovule seed complex being derived entirelyfrom the epi-
with the micropyle protruding(fig. 47). The tip matium. In P. ferruginea, similar conditions ap-
of the bract remains free of the epimatium; oth- ply except that there is normally only a single
erwise epimatium and bractare intimately fused, fertile complex that appearspseudoterminal(fig.
which is pronouncedat seed maturity.The swol- 62). The bractremainsfreeof the rest of the ovule
len bases of the extendedbractsbecome the fleshy complex, and there is little intercalaryextension
receptacle of the mature seed-containing cone, as the seed matures.
which is red and warted and supports the black That the general configuration of the young
epimatium-bract-seedcomplex, togetherwith the complex is virtually identical in cones of very
black tips of the sterile bracts. differentconstructionis illustratedby Dacrydium
cupressinum(fig. 63) and Podocarpusnivalis (fig.
OTHERTAXA (FGS. 52-64). In Halocarpus 64), both of which are representedby cones (ter-
kirkii (figs. 52-55) the epimatium is initiated in minal in the former, lateral in the latter) that
the bract axil as a shallow, laterally extended usually have a single ovule. At comparablestages
mound that soon becomes wider than high (fig. of development, the bract remains free of the
52). The ovule is initiated on the adaxial side of concentriclayers of epimatium, integument, and
the epimatium and is most obvious when nucel- nucellus.A differenceis that the ovule in Dacrydi-
lus and integumentfirstbecome differentiated(fig. um remains more erect (fig. 63) than in Podocar-
53). Bractmaturationis basipetalbut without the pus (fig. 64). This translatesinto contrastedcone
marked intercalaryextension of the bract base, structureat seed maturity.In Dacrydiumthe epi-
as found in Dacrycarpus;epimatium and bract matium remains little developed and forms an
remain discrete (fig. 54). Epimatium enlargement oblique collar aroundthe base of the seed, which
involves the formationof the characteristiclobed itself becomes more erect. At maturitythe black
margin of this species and the engulfmentof the seed coat is contrastedwith the fleshiness of the
ovule, which becomes inverted (figs. 54, 55). Ap- epimatium, but particularlythe bases of the sub-
proaching pollination, only the apex of the in- tending fertile and sterile bracts. In P. nivalisthe
tegument, forming the micropyle, protrudes;the epimatium encloses the mature seed, and the
ovule is fully inverted (fig. 55). fleshyreceptacleis formedby the bases of the two
In Lepidothamnus laxifolius (figs. 56-59), a bracts, even if only one is fertile.
similar sequence of events is illustrated, except
that the ovule remains obliquely erect. In this
species the epimatium remains free of the bract Discussion
distally (figs. 56, 57) but also free of the ovule. The present study demonstrates that the di-
Nucellus and integumentareinitiatedin the usual versity of cone morphologyin Podocarpaceaeis,
way, appearing as concentric ridges within the for the most part, based on a consistent unit that
epimatium (fig. 56). The epimatium encirclesthe involves a uniovulate complex in the axil of each
ovule incompletely and progressively forms a fertilebract.The complex consists of an epimati-
hooded structure, which envelopes the base of um, originating as an axillary structure, which
the ovule (figs. 57, 58). The integument extends develops an adaxial orthotropous ovule. Ovule
beyond this hood, flaringat the mouth in a trum- orientationis usuallyinverted by unequalgrowth
pet-like micropyle that eventually becomes of the epimatium. Thus the unit seems to have
hooked distally (figs. 58, 59). At pollination this a consistent structuraland developmental foun-
inverted orientation of the micropyle projects it dation, although there is considerablevariation,
downward in the cavity enclosed by the bracts, especially in late stages so that the epimatium
into which the pollination drop is secreted. In- may or may not continue to enclose the seed.

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i1~~~~~~~~~6
w - - F<~~~~~~~?*.it -?e

F55
pr~ ~ ~~~~~6

h /1

Figs.52-64 VariousPodocarpaceae,aspectsof cone development.Figs. 52-55, Halocarpuskirkii.Fig. 52, Young bractwith


epimatium in its axil. Fig. 53, Epimatiumwith well-differentiatedovule. Fig. 54, Later stage with epimatium beginningto
invertthe ovule and envelop it. Fig. 55, The lobed marginof the epimatiumpronounced.Figs. 56-59, Lepidothamnuslaxifolius.
Fig. 56, Epimatiumwith young obliquelyerect ovule, overarchedby hooded bracttip. Fig. 57, Laterstage with less elaborate
bract. Fig. 58, Complex with hooded bract;epimatiumincompletelyenvelopingthe more or less erect ovule with integument
beginningto extend.Fig. 59, Cone from side at aboutstageof pollination,the obliquelyerectovule envelopedby the epimatium
with the characteristichooked micropyle.Figs. 60, 61, Prumnopitystaxiifohia.Fig. 60, Epimatiumbeforeovule initiation from
abaxial (outer) side; subtendingbract removed; early evidence of the characteristicbilobed tip of the epimatium. Fig. 61,
Epimatium from adaxial (inner) side with well-developedovule becoming inverted and enveloped by epimatium. Fig. 62,
PrumnopitysfJerruginea, apex of cone from side with pseudoterminalcomplex, the ovule invertedand becomingenvelopedby
the epimatium,the subtendingbractfreefromthe epimatium.Fig. 63, Dacrydiumcupressinum,epimatiumbeginningto envelop

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TOMLINSON -PODOCARP CONE DEVELOPMENT 585

Variationin cone morphologyitself primarilyre- lated characteristicsthat cannot be studied in-


lates to the numbers of fertile units involved but dependently.
is further modified according to the extent to The present study has added a phenological
which other structures,especially bracts, are in- and morphologicaldimension to our knowledge
corporatedinto the maturedisseminule. Much of of the reproductivebiology of podocarpsby dem-
this variation is related, in turn, to the position onstratinga fairly close correlationamong cone
of the cone on the parent shoot, either terminal position, periodicity of shoot extension, and rel-
or lateral,and its time of initiation in relation to ative timing of shoot and cone extension. These
shoot extension,eitherprolepticor sylleptic(Halle additionalfactorsmay influencenumberof cones
et al. 1978). Developmental variation can be and hence reproductiveoutput. A primary con-
traced fartherto the timing and extent of inter- trast is between the location of cones either ter-
calary extension of bracts and cone axis. Where minallyon preexistingvegetativeshoots, i.e., with
extension begins early, for example, bract and a direct transformationof vegetative into repro-
epimatium are intimately fused; where it occurs ductive apices, or as lateralunits on current-year
late, bract and epimatium remain separate and shoots, i.e., with the usual induction of a meri-
grow independentlyin size. stem as a separatereproductiveaxis from its in-
The majorityof generacorrespondto this gen- ception (even though early stages of vegetative
eralizedscheme, but Microstrobosand Phyllocla- and reproductivebranches may be morphologi-
dus are anomalous in their erect ovules and ab- cally indistinguishable). These contrasted con-
sence of an epimatium. No information is ditions are strongly correlated with the type of
available for Microstrobos.In Phyllocladus the adult foliageleaf since lateralcones are associated
aril that develops in the seed arises basally and with linear leaves that are flattened in the hori-
very late so that it is not a feature of the ovule zontal plane, e.g., Afrocarpus,Nageia, Podocar-
at pollination (Tomlinson et al. 1989). Its ho- pus, Prumnopitys,and Sundacarpus,while ter-
mologies are obscure, althoughits function as an minal cones are associated with awl-shaped,
attractantin seed dispersal seems clear. In other scalelike, or linear leaves flattenedin the vertical
taxa the consistent presenceof an epimatium and plane, e.g., Acmopyle, Dacrycarpus,Dacrydium,
its usual role in not only giving rise to and en- Falcatifolium, Halocarpus, Lepidothamnus,and
closing the ovule but also producingan inverted Microcachrys.The lack of specializedcone-bear-
orientationat pollination supportsthe suggestion ing axes in this group is expected because shoots
of Tomlinson et al. (1991) that the primaryfunc- are deterministic in their branchingpattern as a
tion of the epimatium relates to pollination result of syllepsis and the absence of discretely
(Tomlinson 1991). Pollen scavenging by an ex- articulate growth. Such shoot systems lack the
tended pollination drop seems to increase the opportunistic branch expression found in taxa
chances of successful pollination, an important that can sequesterreserve or latent meristems, a
factorin a family in which seed numberper cone consequence of a combination of articulate
is reducedin favor of increasedseed size, in turn growth,scalyterminalbuds, and pronouncedsea-
related to animal dispersal of disseminules that sonal flushes of shoot extension. In the former,
includeboth attractants(color)and rewards(sweet cone numberis determinedby vegetativebranch-
flesh)as illustratedin Salmon (1980). These con- ing, in the latter, it is independent of vegetative
siderationsadvance the comparativestudy of the branching. Exceptions to this generalizationdo
ovulate complex in podocarps beyond that of a occur.Both Decussocarpusand Saxegothaeahave
simple searchfor homologies. The typologicalse- terminalcones but also possess linearleaves. The
ries that can be drawn up-beginning with Mi- shoot morphologyof Decussocarpusis, however,
crocachrys,with many (up to 20) ovules per cone, highly specialized with dimorphic branches.
and ending with the condition in several genera (Tomlinson, unpublished).Saxegothaea, despite
with a single pseudoterminal ovule-does not its advanced method of pollination (Doyle and
necessarilydemonstrate an evolutionary lineage O'Leary 1935; Noren 1908) has a very general-
but provides a basis for comparative study. The ized architecture.
family Podocarpaceaemay thus provide a good In taxa with lateral cones there is furthervari-
example of the value of efficientpollination pro- ation accordingto whether these develop by syl-
cesses in the evolution of the seed habit (Haig lepsis, as in Podocarpus,or prolepsis, as in other
and Westoby 1989) and evidence that reproduc- genera. These considerationsalso govern the in-
tive biology in plants is a syndrome of interre- trinsic morphology of the cone in features that

the well-developedovule. Fig. 64, Podocarpusnivalis, young ovule, inverted and enveloped by growthof epimatium;tip of
bract remainingfree of epimatium (cf. fig. 40). Labelingas in figs. 29-40. Bars = 200 ,umin figs. 52-54 and 60, 61, 63, and
64; 500 ,umin figs. 55-59 and 62.

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586 INTERNATIONAL JOURNAL OF PLANT SCIENCES

parallel those in vegetative shoots (Halle et al. of the seed-scalecomplex" as the initial structure
1978). Syllepticcones (Podocarpus)have a longer that I have called epimatium from the start (figs.
or shorternaked peduncle (or hypopodium) and 65A, 66A). In Stoffberg'sanalysis,this is followed
few bracts(two to six); the prophyllsmay be fer- by the differentiationof the nucellus, priorto the
tile. In contrast,prolepticcones have an extended formation of the integument. Once the ovule is
basal scale-bearingaxis, with numerous sterile clearly circumscribed the epimatium becomes
appendagesbut from as few as one to as many recognizableas the remaining,unspecializedtis-
as 12 fertile appendages. sue of the complex (fig. 65B-E). Differentiation
A furthercomplicationthat has importanteco- of parts is thus intrinsicallybasipetal.
logical consequencesis the intervalbetween cone In contrast, I interpretthe primordium of the
and seed maturation.In Prumnopitysspecies this whole complex as the epimatium on which the
period may be 3 yr and can be contrasted with ovule develops subsequently(fig. 66). The ovule
Phyllocladusin which the whole cycle occurs in primordiumis then the first protuberanceof the
one growingseason. Othertaxa fall betweenthese adaxial side of the epimatium (fig. 66B, C); sub-
extremesand are usuallydescribedas having 1-yr sequently the integument is differentiatedas a
or 2-yr cycles (table 2), althoughthis period does collar-likeoutgrowthwithin the originallimits of
not usuallyconsiderthe additionaltime fromcone the ovule primordiumand well within the outer
induction, which can take up to 6 mo. Gymno- margin of the original epimatium (fig. 66D, E).
spermouslife cyclesare usuallydescribedin terms Development of parts is intrinsically acropetal.
of the appearance of visible structures (Singh Evidence comes from the close series of stages
1977). presentedin the illustrationsof Podocarpus(figs.
With specificreferenceto cone development in 29-40) and Dacrycarpus(figs. 41-51) in which
Podocarpaceaeprevious studies are very limited the integument clearly is generated around the
and not without controversy. Eichler(1873) and rim of the ovular protuberance(esp. figs. 33-36).
Strasburger(1873) debatedwhetherconiferswere A particulartelling piece of evidence is the ini-
genuinely gymnospermouson the basis of an in- tiation of the lobes of the epimatium margin be-
terpretationof the coniferous cone in terms of a fore the appearanceof the ovule primordium(fig.
flower (Strasburgerconcluded they were not!). 33). Also, where the adaxial face of the epimati-
Podocarpsplayed a partin this controversysince um bears the imprint of facing primordia this
the epimatium was variously homologized with does not affect the outline of the ovule and in-
a perianth or the second integument of the an- tegument, which arises later (fig. 50). Stofiberg's
giospermovule. The primarydistinctionbetween analysisprovides too little documentationof sur-
gymnospermsand angiosperms,so clearlyestab- face morphology at critical stages to supporther
lished by Robert Brown (1827) on the basis of conclusion. Neither is her interpretationof the
the site of pollen reception, was overlooked in sequencesupportedby her excellent photomicro-
these static analyses.However, these Germanau- graphs of sections, since they deal only with the
thors, although they may have examined young plane of cell division involved in the inception
cones first hand, did not document their obser- of the integument. In order to accommodate her
vations. The only modem, detailed study is by analysis, she introduced the terms "epimatium
Stoffberg(1991a, 1991b), who studied Podocar- sensu lato" and "epimatium sensu stricto" (her
pus and Afrocarpusin South Africa, as repre- fig. 27). The latter is simply the inner (adaxial)
sented by P. elongatus, P. heinke/ii, P. latifolius margin of the whole of her seed scale complex
(as Podocarpussect. Podocarpus)and A. falcatus and shows the beginningsof the enclosure of the
(as Podocarpussec. Afrocarpus).A clear distinc- whole ovule, variously shown at differentstages
tion is made between the contrastedtypes of cone in differenttaxa in my own surfacephotographs
organization (figs. 6-9, 14) in the two genera, (figs. 29-64). It is inappropriateto make this to-
together with an appreciationfor the differences pographicdistinction if the whole structureis re-
between them in timing of cone formation in re- ferred to as the epimatium, from the start (fig.
lation to shoot extension. The essential topo- 66). This analyticaldifferenceis more than a se-
graphicdetails for Podocarpusare exactly as de- mantic nicety becausein a comparisonwith other
scribed in this paper (figs. 29-40), and the conifers, the epimatium appropriatelymay be re-
description of Afrocarpusfalls within the range gardedas the homologue of the ovuliferous scale
of variation shown for other generaof the family in other conifers, most particularlythe Pinaceae
in the present report (figs. 41-64). (Tomlinson et al. 1991, fig. 38). Evidence for this
However, my interpretationof the sequenceof in my interpretation of an acropetal develop-
events in ovule initiations (figs. 65, 66) differs mental sequence is that the epimatium does in-
totally from that of Stoffberg(1991a, 1991b). Her deed support the ovule. In Stoffberg'sinterpre-
description refers to basipetal development of tation, the ovule appendage would precede the
parts within the ovuliferous complex, beginning axis that morphologically supports it. That this
with a noncommital referenceto a "primordium is not entirelyimpossible is suggestedin the Tax-

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TOMLINSON -PODOCARP CONE DEVELOPMENT 587

int.
nuc.
s.s c.
S.C. nuABASIPETAL

A B C D E

int.

ep. ep. ACROPETAL

A B C D E

br. lint(.g

ep.7
nuep

A B C D E

ep.

br.

Figs.65-67 Fig. 65, Development of the ovuliferous complex in Podocarpaceae with basipetal origin of parts, as implied in
the analysis by Stoffberg (I199lb). A, Establishment of primordium of "seed scale complex" (s. s. c.). B, Initiation of nucellus on
adaxial side of primordium. C, Nucellus (nuc) evident. D, Initiation of integument. E, All parts elaborated, the epimatium (ep)
now regarded as distinct from the ovule. Fig. 66, Development of the ovuliferous complex in Podocarpaceae with acropetal
origin of parts (this paper). A, Initiation of primordium of epimatium (ep). B, Ovule initiation on adaxial side of epimatium.
C, Ovule primordium (ov) evident on epimatium (ep). D, Initiation of integument. E, Integument (int) evident and delimiting
nucellus (nuc) from epimatium (ep). Fig. 67, Distribution of growth centers in the developing ovulate complex in Podocarpaceae
(cf. fig. 66). A, Bract (br) and epimatium (ep) distinct; stippling indicates region of possible intercalary growth common to bract
and epimatium. B, Initiation of ovule (ov) on adaxial surface of epimatium. C, Differentiation of integument (int) and nucellus
(nuc) within ovule. D, E, Further continued uniform enlargement of the complex; E' same as E but at a smaller scale. F, Region
of abaxial extension of epimatium, resulting in inversion of ovule. G, Later stage, with epimatium exceeding bract. H, Final
stage (at pollination) with only the micropyle of the ovule protruding beyond the enveloping epimatium. Later enlargement of
the seed may involve further growth in the hatched region. Different podocarps vary in the extent and timing of these growth
activities, producing very different end products.

odiaceae, where comparative study of the range presentlimited level of understandingis perhaps
of structurespresentedcan lead to the conclusion premature. If one accepts the common ground
that in development appendageprecedes axis in plan as a structuralbasis for understandingdi-
certaintaxa (Takasoand Tomlinson 1989, 1990, versity of podocarp cones, a profitable field for
1992) or that appendage(ovule) and axis (tooth) investigationis the variation in time of initiation
arederived from a common primordium(Takaso of growthprocesses.A hypotheticalseriesof stages
and Tomlinson 1989). of development of a single complex in median
A search for hypothetical homologies at our longitudinal section shows the initiation of the

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588 INTERNATIONAL JOURNAL OF PLANT SCIENCES

epimatium (ep.) in the axil of the bract (br.)with Explorationof the National GeographicSociety.
the futurepersistentmeristematicregionstippled Assistance in collectingwas provided by John E.
(fig. 67A). Subsequentdevelopment of the ovule Braggins,EwenK. Cameron,JackA. Rattenbury,
(ov., fig. 67B) and of the integument (int.) and all of the University of Auckland;Alison Shap-
nucellus (nuc.)proceedspriorto expansion of the cott, University of Tasmania; Chris J. Quinn,
basal region (fig. 67C). Subsequentenlargement University of New South Wales; Jean-Marie
involves activity of this basalmeristematicregion Veillon, ORSTOM, Noumea, New Caledonia;
(fig. 67D-E) as well as the abaxial extension of and N. Kawakubo,Kagoshima University. Sax-
the epimatium (double arrowin fig. 67F, G). Ul- egothaea was collected from cultivated speci-
timately the micropylecomes to have the inverse mens in Irelandwith the help of Jim White, Uni-
orientation seen at the time of pollination (fig. versity College, Dublin. SEM assistance was
67H). Histological analysis of these stages will provided by Robin Pinto (Museum of Compar-
be reportedat a later date. ative Zoology, Harvard University) and by Jim
Walker and Erika Musante (University of Mas-
Acknowledgments sachusetts).TokushiroTakasoassistedwith SEM
Fieldwork in the South Pacific was supported techniques, and Ellen Moriartypreparedthe line
by a grantfrom the Committee on Researchand drawings.

Literature
cited
Brown,R. 1827. Characterand descriptionof Kingia:a new Posluszny,U., M. G. Scott, and R. Sattler. 1980. Revisions
genus of plantsfound on the south-westcoast of New Hol- in the techniquesof epi-illuminationlight microscopyfor
land, with observationson the structureof its unimpreg- the study of floral and vegetative apices. Can. J. Bot. 58:
nated ovulum, and on the female flowerof Cycadeaeand 2491-2495.
Coniferae. Reprinted from Narrative of a survey of the Salmon, J. T. 1980. The native trees of New Zealand.A.
intertropicaland Western Coasts of Australiaperformed H. & W. Reed, Wellington.
between the years 1818 and 1822, CaptainPhilip P. King Singh,H. 1977. The embryologyof gymnosperms.Springer
R.N., F.R.S., F.L.S., vol. 2. London. Verlag,Berlin.
De Laubenfels,D. J. 1972. Flore de la Nouvelle Caledonie Stoffberg,E. 1991a. Morphologicaland ontogeneticstudies
et Dependances.Vol.4. Gymnospermes.MuseumNational on southern African podocarps. Shoot apex morphology
d'HistoireNaturelle,Paris. and ovuliferouscone initiation. Bot. J. Linn. Soc. 105:1-
. 1988. Coniferalesin Flora Malesiana.Ser. 1, vol. 19.
10(3). Nijhoff, The Hague. 1991b. Morphologicaland ontogenetic studies on
Doyle, J. 1945. Developmental lines in pollinatingmech- southern African podocarps. Initiation of the seed scale
anisms in the Coniferales.Sci. Proc. R. Dublin Soc. Ser. A complex and early development of integument, nucellus
24:43-62. and epimatium. Bot. J. Linn. Soc. 105:21-35.
Doyle, J., and M. O'Leary. 1935. Pollination in Saxego- Strasburger,E. 1873. Sind die ConiferenGymnospermen
thaea. Sci. Proc. R. Dublin Soc. 21:175-179. oder nicht?Flora (Regensburg)56:369-377.
Eichler,A. W. 1873. Sind die Coniferengymnospermoder Takaso, T., and P. B. Tomlinson. 1989. Aspects of cone
nicht?Flora (Regensburg)56:3-21. and ovule ontogenyin Cryptomeria(Taxodiaceae).Am. J.
Florin,R. 1954. The femalereproductiveorgansof conifers Bot. 76:692-705.
and taxads. Biol. Rev. 29:367-389. 1990. Cone and ovule ontogeny in Taxodiumand
Haig, D., and M. Westoby. 1989. Selective forces in the Glyptostrobus(Taxodiaceae-Coniferales). Am. J. Bot. 77:
emergenceof the seed habit. Biol. J. Linn. Soc. 38:215- 1209-1221.
238. . 1992. Seed cone and ovule ontogeny in Metase-
Halle, F., R. A. A. Oldeman, and P. B. Tomlinson. 1978. quoia, Sequoia and Sequoiadendron(Taxodiaceae-Conif-
Tropicaltreesand forests:an architecturalanalysis.Spring- erales).Bot. J. Linn. Soc. 108:15-37.
er Verlag,Heidelbergand New York. Tomlinson, P. B. 1991. Pollen scavengingas a novel repro-
Noren, C. 0. 1908. ZurKenntnisder Entwicklungvon Sax- ductive mechanism in Podocarpaceae.Nat. Geog. Res. 7:
egothaeaconspicuaLindl. Sven. Bot. Tidskr. 2:101-122. 188-195.
Page,C. N. 1989. New and maintainedgenerain the conifer Tomlinson, P. B., J. E. Braggins,and J. A. Rattenbury. 1991.
families Podocarpaceaeand Pinaceae.Notes R. Bot. Gard. Pollinationdrop in relationto cone morphologyin Podo-
Edinb. 45:377-395. carpaceae:a novel reproductivemechanism. Am. J. Bot.
. 1990. Coniferophytina(Conifersand Ginkgoids). 78:1289-1303.
Pages279-361 in K. Kubitzki,ed. The familiesand genera Tomlinson, P. B., T. Takaso, and J. A. Rattenbury. 1989.
of vascularplants. Vol. 1. SpringerVerlag,Heidelbergand Cone and ovule ontogenyin Phyllocladus(Podocarpaceae).
New York. Bot. J. Linn. Soc. 99:209-221.

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