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
Stable URL: http://www.jstor.org/stable/2995580 .
Accessed: 03/07/2014 16:12

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp

.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.

The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to
International Journal of Plant Sciences.

http://www.jstor.org

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
 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-

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
 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
fertile (fig. 40). In all cones, the cone apex itself
is consumed in the formation of the ultimate ap-
pendages.
Where lateralcones are producedby prolepsis
(figs. 10-13), the cone is always more elaborate
than in Podocarpusin terms of the largernumber
of appendages.There is always a lateral pair of
prophylls(correspondingto those of a vegetative
branch) and a longer or shorter series of sterile

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
580 INTERNATIONAL JOURNAL
reduced,sterilebractsthat may form a cap to the
cone. In D. dacrydioidesthere is only one, less
commonly two, fertile bracts, and the cone is
distinguishedby the long interval between bract
initiation and final cone maturation, to be de-
scribed later (table 1). All other taxa illustrated
(figs. 25-28) normallyhave only one fertilebract.
There may be sterile reduced bracts above this
as in Lepidothamnus(fig. 24). Otherwisethe sol-
itary ovule is pseudoterminal.In Lepidothamnus
the regularphyllotaxis of distal bracts is some-
what distortedto producea sterilebractopposite
the fertile one, an important component of the
pollinatingmechanism. In Decussocarpuscomp-
tonii the cones are usually terminal,but if lateral
the basal pair of scales is in a prophyllarposition
(dotted outline in fig. 28). The reduction series
appearsto culminate in the taxa with pseudoter-
minal ovules, Acmopyle(not illustrated),Parasi-
taxus (fig. 25), Dacrydium (fig. 26) and Falcati-
folium (fig. 27). The best candidatefor a terminal
ovule complex is D. comptonii,but developmen-
tal stages have not been observed.
CONE DEVELOPMENT
PODOCARPUS
ELATUS
(FIGS.29-40). Cones are
initiatedin the mannerof axillaryvegetativebuds
in association with lower leaves of each renewal
shoot (fig. 5). The precise time of initiation is not
known since it occurs within the restingterminal
bud at the end of a previous unit of shoot exten-
sion. Earlystages of vegetative and reproductive
buds seem identical, but the two become distin-
guishable after the development of the ultimate
(secondor third)pair of appendages.These stages
occur as the parent vegetative axis begins to ex-
tend following bud burst. Initially, the prophylls
arewell advancedin development and exceed the
second pair,in which one or both bractsarefertile
(figs. 8, 9). In figures30-40, the development of
only one fertile complex is followed; the facing
bract, either sterile or fertile, is removed. The
epimatium is initiated in the axil of the fertile
bract as a narrowelongated mound of tissue (fig.
30) that enlargesin proportionto the increasein
size of its subtending bract but becoming nar-
rowed at the base (fig. 31). The apex of the bract
usually becomes hooded and lobed, overarching
the epimatium (figs.32-34). The epimatium may
at firstappearconcave or irregularlylobed, seem-
ingly the result of the pressureof facing append-
ages. First evidence for the development of the
ovule is the appearanceofa centralshallowmound
on its adaxial side (figs. 32, 33). The integument
becomes differentiatedfrom the nucellus(figs.34-
36) in association with the widening of the epi-
matium, which also becomes thickened radially,
i.e., in the adaxial-abaxial plane. At this stage
also, the outermarginof the epimatiummay show
This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM
All use subject to JSTOR Terms and Conditions
OF PLANT SCIENCES
the inception of irregularshallow lobes (figs. 35-
37). In furtherdevelopment the common base of
epimatium and bract begins to extend (fig. 37),
the integument becomes more pronounced (figs.
36, 37), and the abaxial surfaceof the epimatium
extends and forces the ovule into an increasingly
inverted position (fig. 37). The distal (adaxial)
marginof the epimatium continues to grow, pro-
gressivelyenclosingthe ovule (fig.38). Laterstages
show a markedextensionof the epimatium,which
soon exceeds the limits of the subtendingbract,
the enclosure of the ovule, so that the nucellus is
obscured, by the enlargement, both axially and
radially of the common base of the epimatium
and bract (fig. 39). At the time of pollination the
upperbractsmuch exceed the prophyllsand show
the enlargementthat presagestheir swollen con-
dition at seed maturity. The epimatium exceeds
its subtendingbract, its apex is pointed (fig. 40),
and the integument is completely enclosed, ex-
cept for the protrudingmouth of the micropyle
(figs. 39, 40).
DACRYCARPUS DACRYDIOIDES (FIGS. 41-
51). This species is distinguished by the bi-
modal sequenceof cone development.Earlystages
of cone initiation up to the formation of the two
to three robust bracts, can be found as early as
March (late summer). The cone remains in this
condition until September,when epimatium and
ovule initiation and bract extension begin, pro-
ceeding within 3-4 wk to cone maturationas far
as the stage of pollination. Figures 41-44 show
the transition from vegetative to reproductive
apices and the initiation of bracts;figures45-47
show the entirecone duringepimatiumand ovule
development, while figures48-51 show stages in
the initiation of the ovule.
Vegetative shoots have a pronounced dome-
shaped apex above the insertion of the youngest
visible leaf primordia (figs. 41, 42). The size of
the apex and phyllotaxis are determined by the
vigor of the shoot; higherorderaxes on any shoot
complex are always smallest. Reproductive api-
ces can most easily be identified,upon dissection,
by the two to three bract primordia that intrin-
sically consume the apex (fig. 43). These bracts
proceed to a stage when they are short but thick-
ened radiallyand contrast with the primordiaof
the foliage leaves immediately below (fig. 44). In
this condition the cones overwinter with a rela-
tively inactive period of about 5 mo. Renewed
developmentin Augustis indicatedby intercalary
extension of the bract bases and the initiation-
above the axil of one of them (sometimes two)-
of the epimatium as a low mound of tissue (fig.
45). There is rapid extension of the bracts (fig.
46) mainly by intercalarygrowthso that the ovu-
lar complex is carried up on the adaxial face of
the bract(fig. 47). Examinationof individual fer-
 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.

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
 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.

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
 TOMLINSON-PODOCARP
tile complexes shows the inception of the epi-
matium on the adaxial face of the bract as a low
protuberance(fig.48). This enlargesand is carried
up by the expansion and extension of the bract
base so that it soon appearsto be situated on the
adaxial face of the bract (fig. 49). It may appear
lobed because of the pressureof the facing sterile
bracts(fig. 50). Integumentdifferentiationdelim-
its the nucellus.This is clearlywithin the confines
of the epimatium since the prior lobing does not
significantlyinfluence the outline of the integu-
ment (fig. 50). With furtheruniform enlargement
of the complex, nucellus (n), integument (i), epi-
matium (e), and bract (b) are discretelyseparated
(fig. 51). Later expansion of the epimatium in-
volves the enclosure and inversion of the ovule
with the micropyle protruding(fig. 47). The tip
of the bract remains free of the epimatium; oth-
erwise epimatium and bractare intimately fused,
which is pronouncedat seed maturity.The swol-
len bases of the extendedbractsbecome the fleshy
receptacle of the mature seed-containing cone,
which is red and warted and supports the black
epimatium-bract-seedcomplex, togetherwith the
black tips of the sterile bracts.
OTHERTAXA (FGS. 52-64). In Halocarpus
kirkii (figs. 52-55) the epimatium is initiated in
the bract axil as a shallow, laterally extended
mound that soon becomes wider than high (fig.
52). The ovule is initiated on the adaxial side of
the epimatium and is most obvious when nucel-
lus and integumentfirstbecome differentiated(fig.
53). Bractmaturationis basipetalbut without the
marked intercalaryextension of the bract base,
as found in Dacrycarpus;epimatium and bract
remain discrete (fig. 54). Epimatium enlargement
involves the formationof the characteristiclobed
margin of this species and the engulfmentof the
ovule, which becomes inverted (figs. 54, 55). Ap-
proaching pollination, only the apex of the in-
tegument, forming the micropyle, protrudes;the
ovule is fully inverted (fig. 55).
In Lepidothamnus laxifolius (figs. 56-59), a
similar sequence of events is illustrated, except
that the ovule remains obliquely erect. In this
species the epimatium remains free of the bract
distally (figs. 56, 57) but also free of the ovule.
Nucellus and integumentareinitiatedin the usual
way, appearing as concentric ridges within the
epimatium (fig. 56). The epimatium encirclesthe
ovule incompletely and progressively forms a
hooded structure, which envelopes the base of
the ovule (figs. 57, 58). The integument extends
beyond this hood, flaringat the mouth in a trum-
pet-like micropyle that eventually becomes
hooked distally (figs. 58, 59). At pollination this
inverted orientation of the micropyle projects it
downward in the cavity enclosed by the bracts,
into which the pollination drop is secreted. In-
This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM
All use subject to JSTOR Terms and Conditions
CONE DEVELOPMENT 583
tercalaryextension of the bases of the bracts ex-
tends the whole unit on a common axis (fig. 59).
The seed remains naked and erect at maturity,
with the epimatium forming a short lobed collar
at its base. Subtendingsterilebractsbecome fleshy.
In P. taxifolia, the epimatium is an axillary
structure(fig. 60). This is a view of the abaxial
side with the subtending bract removed. In this
species there is little intercalaryextension of the
complex so that bractand epimatium remaindis-
crete. The ovule is initiated on the adaxial side
of the bract in the usual way (fig. 61), the epi-
matium much exceeding the young ovule, which
is consequentlyinverted from the start.The bract
plays no part in dispersal, the fleshy layer of the
seed complex being derived entirelyfrom the epi-
matium. In P. ferruginea, similar conditions ap-
ply except that there is normally only a single
fertile complex that appearspseudoterminal(fig.
62). The bractremainsfreeof the rest of the ovule
complex, and there is little intercalaryextension
as the seed matures.
That the general configuration of the young
complex is virtually identical in cones of very
differentconstructionis illustratedby Dacrydium
cupressinum(fig. 63) and Podocarpusnivalis (fig.
64), both of which are representedby cones (ter-
minal in the former, lateral in the latter) that
usually have a single ovule. At comparablestages
of development, the bract remains free of the
concentriclayers of epimatium, integument, and
nucellus.A differenceis that the ovule in Dacrydi-
um remains more erect (fig. 63) than in Podocar-
pus (fig. 64). This translatesinto contrastedcone
structureat seed maturity.In Dacrydiumthe epi-
matium remains little developed and forms an
oblique collar aroundthe base of the seed, which
itself becomes more erect. At maturitythe black
seed coat is contrastedwith the fleshiness of the
epimatium, but particularlythe bases of the sub-
tending fertile and sterile bracts. In P. nivalisthe
epimatium encloses the mature seed, and the
fleshyreceptacleis formedby the bases of the two
bracts, even if only one is fertile.
Discussion
The present study demonstrates that the di-
versity of cone morphologyin Podocarpaceaeis,
for the most part, based on a consistent unit that
involves a uniovulate complex in the axil of each
fertilebract.The complex consists of an epimati-
um, originating as an axillary structure, which
develops an adaxial orthotropous ovule. Ovule
orientationis usuallyinverted by unequalgrowth
of the epimatium. Thus the unit seems to have
a consistent structuraland developmental foun-
dation, although there is considerablevariation,
especially in late stages so that the epimatium
may or may not continue to enclose the seed.
 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

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
 TOMLINSON -PODOCARP
Variationin cone morphologyitself primarilyre-
lates to the numbers of fertile units involved but
is further modified according to the extent to
which other structures,especially bracts, are in-
corporatedinto the maturedisseminule. Much of
this variation is related, in turn, to the position
of the cone on the parent shoot, either terminal
or lateral,and its time of initiation in relation to
shoot extension,eitherprolepticor sylleptic(Halle
et al. 1978). Developmental variation can be
traced fartherto the timing and extent of inter-
calary extension of bracts and cone axis. Where
extension begins early, for example, bract and
epimatium are intimately fused; where it occurs
late, bract and epimatium remain separate and
grow independentlyin size.
The majorityof generacorrespondto this gen-
eralizedscheme, but Microstrobosand Phyllocla-
dus are anomalous in their erect ovules and ab-
sence of an epimatium. No information is
available for Microstrobos.In Phyllocladus the
aril that develops in the seed arises basally and
very late so that it is not a feature of the ovule
at pollination (Tomlinson et al. 1989). Its ho-
mologies are obscure, althoughits function as an
attractantin seed dispersal seems clear. In other
taxa the consistent presenceof an epimatium and
its usual role in not only giving rise to and en-
closing the ovule but also producingan inverted
orientationat pollination supportsthe suggestion
of Tomlinson et al. (1991) that the primaryfunc-
tion of the epimatium relates to pollination
(Tomlinson 1991). Pollen scavenging by an ex-
tended pollination drop seems to increase the
chances of successful pollination, an important
factorin a family in which seed numberper cone
is reducedin favor of increasedseed size, in turn
related to animal dispersal of disseminules that
includeboth attractants(color)and rewards(sweet
flesh)as illustratedin Salmon (1980). These con-
siderationsadvance the comparativestudy of the
ovulate complex in podocarps beyond that of a
simple searchfor homologies. The typologicalse-
ries that can be drawn up-beginning with Mi-
crocachrys,with many (up to 20) ovules per cone,
and ending with the condition in several genera
with a single pseudoterminal ovule-does not
necessarilydemonstrate an evolutionary lineage
but provides a basis for comparative study. The
family Podocarpaceaemay thus provide a good
example of the value of efficientpollination pro-
cesses in the evolution of the seed habit (Haig
and Westoby 1989) and evidence that reproduc-
tive biology in plants is a syndrome of interre-
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.
This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM
All use subject to JSTOR Terms and Conditions
CONE DEVELOPMENT 585
lated characteristicsthat cannot be studied in-
dependently.
The present study has added a phenological
and morphologicaldimension to our knowledge
of the reproductivebiology of podocarpsby dem-
onstratinga fairly close correlationamong cone
position, periodicity of shoot extension, and rel-
ative timing of shoot and cone extension. These
additionalfactorsmay influencenumberof cones
and hence reproductiveoutput. A primary con-
trast is between the location of cones either ter-
minallyon preexistingvegetativeshoots, i.e., with
a direct transformationof vegetative into repro-
ductive apices, or as lateralunits on current-year
shoots, i.e., with the usual induction of a meri-
stem as a separatereproductiveaxis from its in-
ception (even though early stages of vegetative
and reproductivebranches may be morphologi-
cally indistinguishable). These contrasted con-
ditions are strongly correlated with the type of
adult foliageleaf since lateralcones are associated
with linear leaves that are flattened in the hori-
zontal plane, e.g., Afrocarpus,Nageia, Podocar-
pus, Prumnopitys,and Sundacarpus,while ter-
minal cones are associated with awl-shaped,
scalelike, or linear leaves flattenedin the vertical
plane, e.g., Acmopyle, Dacrycarpus,Dacrydium,
Falcatifolium, Halocarpus, Lepidothamnus,and
Microcachrys.The lack of specializedcone-bear-
ing axes in this group is expected because shoots
are deterministic in their branchingpattern as a
result of syllepsis and the absence of discretely
articulate growth. Such shoot systems lack the
opportunistic branch expression found in taxa
that can sequesterreserve or latent meristems, a
consequence of a combination of articulate
growth,scalyterminalbuds, and pronouncedsea-
sonal flushes of shoot extension. In the former,
cone numberis determinedby vegetativebranch-
ing, in the latter, it is independent of vegetative
branching. Exceptions to this generalizationdo
occur.Both Decussocarpusand Saxegothaeahave
terminalcones but also possess linearleaves. The
shoot morphologyof Decussocarpusis, however,
highly specialized with dimorphic branches.
(Tomlinson, unpublished).Saxegothaea, despite
its advanced method of pollination (Doyle and
O'Leary 1935; Noren 1908) has a very general-
ized architecture.
In taxa with lateral cones there is furthervari-
ation accordingto whether these develop by syl-
lepsis, as in Podocarpus,or prolepsis, as in other
genera. These considerationsalso govern the in-
trinsic morphology of the cone in features that
586 INTERNATIONAL
parallel those in vegetative shoots (Halle et al.
1978). Syllepticcones (Podocarpus)have a longer
or shorternaked peduncle (or hypopodium) and
few bracts(two to six); the prophyllsmay be fer-
tile. In contrast,prolepticcones have an extended
basal scale-bearingaxis, with numerous sterile
appendagesbut from as few as one to as many
as 12 fertile appendages.
A furthercomplicationthat has importanteco-
logical consequencesis the intervalbetween cone
and seed maturation.In Prumnopitysspecies this
period may be 3 yr and can be contrasted with
Phyllocladusin which the whole cycle occurs in
one growingseason. Othertaxa fall betweenthese
extremesand are usuallydescribedas having 1-yr
or 2-yr cycles (table 2), althoughthis period does
not usuallyconsiderthe additionaltime fromcone
induction, which can take up to 6 mo. Gymno-
spermouslife cyclesare usuallydescribedin terms
of the appearance of visible structures (Singh
1977).
With specificreferenceto cone development in
Podocarpaceaeprevious studies are very limited
and not without controversy. Eichler(1873) and
Strasburger(1873) debatedwhetherconiferswere
genuinely gymnospermouson the basis of an in-
terpretationof the coniferous cone in terms of a
flower (Strasburgerconcluded they were not!).
Podocarpsplayed a partin this controversysince
the epimatium was variously homologized with
a perianth or the second integument of the an-
giospermovule. The primarydistinctionbetween
gymnospermsand angiosperms,so clearlyestab-
lished by Robert Brown (1827) on the basis of
the site of pollen reception, was overlooked in
these static analyses.However, these Germanau-
thors, although they may have examined young
cones first hand, did not document their obser-
vations. The only modem, detailed study is by
Stoffberg(1991a, 1991b), who studied Podocar-
pus and Afrocarpusin South Africa, as repre-
sented by P. elongatus, P. heinke/ii, P. latifolius
(as Podocarpussect. Podocarpus)and A. falcatus
(as Podocarpussec. Afrocarpus).A clear distinc-
tion is made between the contrastedtypes of cone
organization (figs. 6-9, 14) in the two genera,
together with an appreciationfor the differences
between them in timing of cone formation in re-
lation to shoot extension. The essential topo-
graphicdetails for Podocarpusare exactly as de-
scribed in this paper (figs. 29-40), and the
description of Afrocarpusfalls within the range
of variation shown for other generaof the family
in the present report (figs. 41-64).
However, my interpretationof the sequenceof
events in ovule initiations (figs. 65, 66) differs
totally from that of Stoffberg(1991a, 1991b). Her
description refers to basipetal development of
parts within the ovuliferous complex, beginning
with a noncommital referenceto a "primordium
This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM
All use subject to JSTOR Terms and Conditions
JOURNAL OF PLANT SCIENCES
of the seed-scalecomplex" as the initial structure
that I have called epimatium from the start (figs.
65A, 66A). In Stoffberg'sanalysis,this is followed
by the differentiationof the nucellus, priorto the
formation of the integument. Once the ovule is
clearly circumscribed the epimatium becomes
recognizableas the remaining,unspecializedtis-
sue of the complex (fig. 65B-E). Differentiation
of parts is thus intrinsicallybasipetal.
In contrast, I interpretthe primordium of the
whole complex as the epimatium on which the
ovule develops subsequently(fig. 66). The ovule
primordiumis then the first protuberanceof the
adaxial side of the epimatium (fig. 66B, C); sub-
sequently the integument is differentiatedas a
collar-likeoutgrowthwithin the originallimits of
the ovule primordiumand well within the outer
margin of the original epimatium (fig. 66D, E).
Development of parts is intrinsically acropetal.
Evidence comes from the close series of stages
presentedin the illustrationsof Podocarpus(figs.
29-40) and Dacrycarpus(figs. 41-51) in which
the integument clearly is generated around the
rim of the ovular protuberance(esp. figs. 33-36).
A particulartelling piece of evidence is the ini-
tiation of the lobes of the epimatium margin be-
fore the appearanceof the ovule primordium(fig.
33). Also, where the adaxial face of the epimati-
um bears the imprint of facing primordia this
does not affect the outline of the ovule and in-
tegument, which arises later (fig. 50). Stofiberg's
analysisprovides too little documentationof sur-
face morphology at critical stages to supporther
conclusion. Neither is her interpretationof the
sequencesupportedby her excellent photomicro-
graphs of sections, since they deal only with the
plane of cell division involved in the inception
of the integument. In order to accommodate her
analysis, she introduced the terms "epimatium
sensu lato" and "epimatium sensu stricto" (her
fig. 27). The latter is simply the inner (adaxial)
margin of the whole of her seed scale complex
and shows the beginningsof the enclosure of the
whole ovule, variously shown at differentstages
in differenttaxa in my own surfacephotographs
(figs. 29-64). It is inappropriateto make this to-
pographicdistinction if the whole structureis re-
ferred to as the epimatium, from the start (fig.
66). This analyticaldifferenceis more than a se-
mantic nicety becausein a comparisonwith other
conifers, the epimatium appropriatelymay be re-
gardedas the homologue of the ovuliferous scale
in other conifers, most particularlythe Pinaceae
(Tomlinson et al. 1991, fig. 38). Evidence for this
in my interpretation of an acropetal develop-
mental sequence is that the epimatium does in-
deed support the ovule. In Stoffberg'sinterpre-
tation, the ovule appendage would precede the
axis that morphologically supports it. That this
is not entirelyimpossible is suggestedin the Tax-
 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
of structurespresentedcan lead to the conclusion
that in development appendageprecedes axis in
certaintaxa (Takasoand Tomlinson 1989, 1990,
1992) or that appendage(ovule) and axis (tooth)
arederived from a common primordium(Takaso
and Tomlinson 1989).
A search for hypothetical homologies at our
presentlimited level of understandingis perhaps
premature. If one accepts the common ground
plan as a structuralbasis for understandingdi-
versity of podocarp cones, a profitable field for
investigationis the variation in time of initiation
of growthprocesses.A hypotheticalseriesof stages
of development of a single complex in median
longitudinal section shows the initiation of the

This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM

All use subject to JSTOR Terms and Conditions
588 INTERNATIONAL JOURNAL
epimatium (ep.) in the axil of the bract (br.)with
the futurepersistentmeristematicregionstippled
(fig. 67A). Subsequentdevelopment of the ovule
(ov., fig. 67B) and of the integument (int.) and
nucellus (nuc.)proceedspriorto expansion of the
basal region (fig. 67C). Subsequentenlargement
involves activity of this basalmeristematicregion
(fig. 67D-E) as well as the abaxial extension of
the epimatium (double arrowin fig. 67F, G). Ul-
timately the micropylecomes to have the inverse
orientation seen at the time of pollination (fig.
67H). Histological analysis of these stages will
be reportedat a later date.
Acknowledgments
Fieldwork in the South Pacific was supported
by a grantfrom the Committee on Researchand
Literature
cited
Brown,R. 1827. Characterand descriptionof Kingia:a new
genus of plantsfound on the south-westcoast of New Hol-
land, with observationson the structureof its unimpreg-
nated ovulum, and on the female flowerof Cycadeaeand
Coniferae. Reprinted from Narrative of a survey of the
intertropicaland Western Coasts of Australiaperformed
between the years 1818 and 1822, CaptainPhilip P. King
R.N., F.R.S., F.L.S., vol. 2. London.
De Laubenfels,D. J. 1972. Flore de la Nouvelle Caledonie
et Dependances.Vol.4. Gymnospermes.MuseumNational
d'HistoireNaturelle,Paris.
. 1988. Coniferalesin Flora Malesiana.Ser. 1, vol.
10(3). Nijhoff, The Hague.
Doyle, J. 1945. Developmental lines in pollinatingmech-
anisms in the Coniferales.Sci. Proc. R. Dublin Soc. Ser. A
24:43-62.
Doyle, J., and M. O'Leary. 1935. Pollination in Saxego-
thaea. Sci. Proc. R. Dublin Soc. 21:175-179.
Eichler,A. W. 1873. Sind die Coniferengymnospermoder
nicht?Flora (Regensburg)56:3-21.
Florin,R. 1954. The femalereproductiveorgansof conifers
and taxads. Biol. Rev. 29:367-389.
Haig, D., and M. Westoby. 1989. Selective forces in the
emergenceof the seed habit. Biol. J. Linn. Soc. 38:215-
238.
Halle, F., R. A. A. Oldeman, and P. B. Tomlinson. 1978.
Tropicaltreesand forests:an architecturalanalysis.Spring-
er Verlag,Heidelbergand New York.
Noren, C. 0. 1908. ZurKenntnisder Entwicklungvon Sax-
egothaeaconspicuaLindl. Sven. Bot. Tidskr. 2:101-122.
Page,C. N. 1989. New and maintainedgenerain the conifer
families Podocarpaceaeand Pinaceae.Notes R. Bot. Gard.
Edinb. 45:377-395.
. 1990. Coniferophytina(Conifersand Ginkgoids).
Pages279-361 in K. Kubitzki,ed. The familiesand genera
of vascularplants. Vol. 1. SpringerVerlag,Heidelbergand
New York.
This content downloaded from 95.94.129.224 on Thu, 3 Jul 2014 16:12:12 PM
All use subject to JSTOR Terms and Conditions
OF PLANT SCIENCES
Explorationof the National GeographicSociety.
Assistance in collectingwas provided by John E.
Braggins,EwenK. Cameron,JackA. Rattenbury,
all of the University of Auckland;Alison Shap-
cott, University of Tasmania; Chris J. Quinn,
University of New South Wales; Jean-Marie
Veillon, ORSTOM, Noumea, New Caledonia;
and N. Kawakubo,Kagoshima University. Sax-
egothaea was collected from cultivated speci-
mens in Irelandwith the help of Jim White, Uni-
versity College, Dublin. SEM assistance was
provided by Robin Pinto (Museum of Compar-
ative Zoology, Harvard University) and by Jim
Walker and Erika Musante (University of Mas-
sachusetts).TokushiroTakasoassistedwith SEM
techniques, and Ellen Moriartypreparedthe line
drawings.
Posluszny,U., M. G. Scott, and R. Sattler. 1980. Revisions
in the techniquesof epi-illuminationlight microscopyfor
the study of floral and vegetative apices. Can. J. Bot. 58:
2491-2495.
Salmon, J. T. 1980. The native trees of New Zealand.A.
H. & W. Reed, Wellington.
Singh,H. 1977. The embryologyof gymnosperms.Springer
Verlag,Berlin.
Stoffberg,E. 1991a. Morphologicaland ontogeneticstudies
on southern African podocarps. Shoot apex morphology
and ovuliferouscone initiation. Bot. J. Linn. Soc. 105:1-
19.
1991b. Morphologicaland ontogenetic studies on
southern African podocarps. Initiation of the seed scale
complex and early development of integument, nucellus
and epimatium. Bot. J. Linn. Soc. 105:21-35.
Strasburger,E. 1873. Sind die ConiferenGymnospermen
oder nicht?Flora (Regensburg)56:369-377.
Takaso, T., and P. B. Tomlinson. 1989. Aspects of cone
and ovule ontogenyin Cryptomeria(Taxodiaceae).Am. J.
Bot. 76:692-705.
1990. Cone and ovule ontogeny in Taxodiumand
Glyptostrobus(Taxodiaceae-Coniferales). Am. J. Bot. 77:
1209-1221.
. 1992. Seed cone and ovule ontogeny in Metase-
quoia, Sequoia and Sequoiadendron(Taxodiaceae-Conif-
erales).Bot. J. Linn. Soc. 108:15-37.
Tomlinson, P. B. 1991. Pollen scavengingas a novel repro-
ductive mechanism in Podocarpaceae.Nat. Geog. Res. 7:
188-195.
Tomlinson, P. B., J. E. Braggins,and J. A. Rattenbury. 1991.
Pollinationdrop in relationto cone morphologyin Podo-
carpaceae:a novel reproductivemechanism. Am. J. Bot.
78:1289-1303.
Tomlinson, P. B., T. Takaso, and J. A. Rattenbury. 1989.
Cone and ovule ontogenyin Phyllocladus(Podocarpaceae).
Bot. J. Linn. Soc. 99:209-221.