Pollination Drop in Relation to Cone Morphology in Podocarpaceae: A Novel Reproductive
Mechanism
Author(s): P. B. Tomlinson, J. E. Braggins, J. A. Rattenbury
Source: American Journal of Botany, Vol. 78, No. 9 (Sep., 1991), pp. 1289-1303
Published by: Botanical Society of America
Stable URL: http://www.jstor.org/stable/2444932 .
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AmericanJournal
ofBotany78(9): 1289-1303. 1991.
POLLINATION DROP IN RELATION TO CONE MORPHOLOGY IN
PODOCARPACEAE: A NOVEL REPRODUCTIVE MECHANISM'
P. B. TOMLINSON,2'4 J.E.
BRAGGINS,3
AND J. A. RATTENBURY3
01366; and
2HarvardForest,Petersham,
Massachusetts
ofBotany,University
ofAuckland,
Auckland,New Zealand
3Department
in thesouthern
family
Observation
of ovulateconesat thetimeof pollination
coniferous
a distinctive
methodof pollencapture,involvingan extended
Podocarpaceaedemonstrates
and singlewithintheaxil
areorthotropous
pollination
drop.Ovulesin all generaofthefamily
ovulesare-erect(i.e., the micropyle
of each fertile
bract.In Microstrobus
and Phyllocladus
structure
directedawayfromtheconeaxis) and are notassociatedwithan ovule-supporting
Pollenin thesetwogeneramustlanddirectly
on thepollination
dropin theway
(epimatium).
In all othergenera,theovuleis inverted
usualforgymnosperms,
as observedin Phyllocladus.
by a specializedovuleis directedtowardthecone axis) and supported
(i.e., themicropyle
In Saxegothaeathereis no pollination
structure
dropandgametesare
(epimatium).
supporting
deliveredto theovulebypollentubegrowth.
Pollination
dropswereobservedin sevenofthe
orconeaxis
remaining
genera.In thesegenerathedropextendsovertheadjacentbractsurface
Thepollen
andcanretainpollenthathas arrivedpriorto dropsecretion
("pollenscavenging").
oftheconeinothergenerainwhich
cavity.Theconfiguration
floatsupwardintothemicropylar
is general
a pollination
thatpollenscavenging
suggests
drophas notyetbeenobserveddirectly
byextending
pollination
in spaceand
efficiency
withinthefamily
andmayincreasepollination
in eachcone,
time.Increasedpollination
ofovulenumber
efficiency
mayrelatetothereduction
thatanimal
oftento onein manygenera,
A biologicalperspective
suggests
a derivedcondition.
theneed
forcethathas generated
adaptivedriving
dispersaloflargeseedsmaybe theultimate
forgreater
efficiency.
pollination
We heredocumentthatthepollination
drop fleshyseeds dispersedby animals (mainly
mechanismofmanymembersofthesouthern birds).
hemisphere
coniferous
familyPodocarpaceae A pollination
dropis knowntobe produced
(podocarps)differs
fromthatin most gym- in all speciesof Cephalotaxaceae,Cupressanosperms.
Thedropcan"scavenge"pollenthat ceae,Taxaceae,andTaxodiaceaethathavebeen
has previouslyfallenneartheovule,priorto studied(Takaso, 1990). In Araucariaceaeno
dropoccurs,thegametesbeingdedropsecretion.Presumably
thisincreasesthe pollination
bypollentubegrowth
with liveredto themicropyle
ofpollinationand is correlated
efficiency
thereducednumberofovulesperconein most (Eames, 1913; Haines, Prakash,and Nikles,
podocarps.The Podocarpaceae,unlikemost 1984). The greatestdiversityin pollination
is knownforPinaceae,in which
otherconifers,are largelycharacterized
by mechanisms
a pollinationdrop is reportedforPicea and
Pinus,whileothergenerahave mechanisms
1 Receivedforpublication
21 January1991; revision without
suchas pollenengulfdropsecretion,
accepted7 May 1991.
(Doyle,1945).AbThe authorsthanktheDirectorsand ChiefRangersof mentorpollentubegrowth
derivedsincethe
of
a
is
considered
drop
sence
Mt. TongariroNationalPark; AucklandRegionalAudropmaybe a very
BotanicalGarden,Manurewa;Waitakere
Conser- presenceof a pollination
thority
vationArea,Auckland;KauaerangaForestReserve,Cor- ancientfeature
(cf.Rothwell,
ofgymnosperms
omandel,all in New Zealand;Mt. Field NationalPark, 1977). In Podocarpaceaetherehas been no
Tasmania;andFairchild
TropicalGarden,Miami,Florida observation
in natmechanisms
ofpollination
inseveral
forpermission
tocollectandmakeobservations
trees.Doyle (1945) suggested
protected
areas;AlisonShapcott,
University
ofTasmania; urallygrowing
a parallelseries
C. J.Quinn,University
ofNewSouthWales;J.-M.Veillon, thatthePodocarpaceaeformed
CentreO.R.S.T.O.M.,Noumea,NewCaledonia;andEwen to thePinaceae,also involvingloss of a polK. Cameron,University
of Aucklandforfurther
collec- linationdrop,but he describeda pollination
and Toku- drop onlyin one specieseach of Podocarpus
tionsand fieldassistance;and EllenMoriarty
Fieldworkin the
shiroTakasoforhelpwithillustrations.
cultivatedin Irishgardens.
SouthPacificwas supported
by a grantto PBT fromthe and Prumnopitys
ResearchCommittee
oftheNationalGeographic
Society. Saxegothaea,whichlacks a pollinationdrop
(Noren,1908;Doyleand O'Leary,1935),was
4Author forcorrespondence.
1289
1290
TABLE
[Vol. 78
AMERICAN JOURNAL OF BOTANY
1.
Podocarpaceae.Taxa withan observed
pollination
drop
Taxon
Dacrycarpusdacrydioides
Halocarpus kirkii
Lagarostroboscolensoi
Lepidothamnusintermedius
Lepidothamnuslaxifolius
Microcachrystetragona
Phyllocladusaspleniifoliusvar. alpinus
Phyllocladustrichomanoides
Podocarpus macrophyllus
Podocarpus nivalis
Podocarpus totara
Prumnopitysandina
Prumnopitysferruginea
Prumnopitystaxifolia
Localityr
Huia (NZ)
Kelly's Road, Waitemata (NZ)
Cult. Auckland Univ. Campus (NZ)
Kauaeranga For. Res. (NZ)
TongariroNat. Park (NZ)
Mt. Field Nat. Park (T)
TongariroNat. Park (NZ)
Cornwall Park, Auckland (NZ)
Cult. Fairchild Tropical Garden (US)
TongariroNat. Park (NZ)
Manurewa Bot. Gard. (NZ)
Cult. Hobart Bot. Gard. (T)
WaitakereHills (NZ)
Manurewa Bot. Gard. (NZ)
a
NZ = North Island, New Zealand, T = Tasmania, US = United States.
b Morphological orientationwith respectto cone axis.
No.
fertile
bracts
1(-2)
2-3
2-3
1(-2)
1(-2)
8-16
1-5
2-7
1-2
1-2
1-2
5-10
1(-2)
5-10
Ovule orientationb
Inverted
Inverted
Inverted
Obliquely erect
Obliquely erect
Inverted
Erect
Erect
Inverted
Inverted
Inverted
Inverted
Inverted
Inverted
weremadeon populations
consideredby Doyle to be highlyderivedand Mostobservations
greatly in theAucklandregionofNewZealand(Table
analogousto Tsuga.Our observations
forPodocarpaceae
andshow 1) sincetheseprovidedconvenientaccess to
amplify
thepicture
drops
Pollination
facilities.
per- photomicrographic
oftheirpollination;
manyuniquefeatures
inthefieldwitha hand
haps onlyin Picea and Pinus,whichhave an canbe observeddirectly
abilityto retainpollenpriorto dropsecretion, lens. Detachedshootswithovulatecones at
mayparallelsbe drawn(Owens,Simpson,and the stageof pollinationwerebroughtinto a
room,keptin water,and enclosedin
Molder,1981; Owens,Simpson,and Caron, sheltered
1987).
a plasticbag. This usuallyresultsin dropseThe Podocarpaceaeincludes18 genera(17 cretionin a normalway.Pollinationdropseis excludedas Phyllocladaceae; cretionis mostlyin thelate evening,and the
ifPhyllocladus
resorbedbylatemorning,
Page, 1990) and about 200 speciesof shrubs dropsare normally
in theGon- but enclosedcut shootscan retaindropsfor
andtrees,witha widedistribution
fresh
tetragona,
dwanaregion,i.e., presentday Africa,south- severaldays.In Microcachrys
and SouthAmerica(De conesflownfromTasmaniato AucklandpereastAsia,Australasia,
of pollinationdrops
Laubenfels,1988). New Caledonia (18 spp.) mittedthe photography
ofconesat the
local in thisway.Microphotography
andNewZealand(17 spp).bothrepresent
andendemism.Plantstyp- stage of pollinationwas done with a Wild
centersofdiversity
icallyoccupymontanehabitatsin thetropics, stereomicroscopeusing Ektachromecolor
film(ASA 100);Figs.1-9, 12-20
of transparency
butin NewZealandarea majorcomponent
fromthese
reproductions
themixedpodocarpforestat all altitudesand areblack-and-white
dominant.Recentgenericre- transparencies.
are frequently
ofovuleswithandwithSomemanipulation
clarified
thestatusofcerhasgreatly
alignment
ofthe outcapturedpollengrainswas doneunderthe
by dismemberment
taingroups,chiefly
Dacryd- microscopeto understandthe mechanicsof
unnatural
genera,
largeandpreviously
ofovuleswith
Reorientation
(e.g.,Tegner,1967;Quinn, pollenmovement.
iumandPodocarpus
thebuoyancyof
1972,1988; enclosedpollendemonstrated
1970,1982,1987;De Laubenfels,
pollenwithinnaturaldrops,or withindrops
Page, 1989, 1990).
simulatedby addingwater.
MATERIALS AND METHODS
RESULTS
trees
Observations
weremadeon field-grown
-An
Coneorientation
Generalmechanismsfromwild and cultivatedpopulationsin the
ofthepollinationmechanism
feature
to December1989,in New intrinsic
periodSeptember
of
Zealand,Tasmania,and New Caledonia.Rec- of mostpodocarpsis theerectorientation
commonly
ognitionofthepollinationprocesswas facili- theconeat thetimeofpollination,
at the-time
curvature
aboutbygrowth
tatedbycontinualmonitoring
ofshootdevel- brought
is an example
ofpodocarpsundertaken theconeexpands.Phyllocladus
opmentina diversity
genusbecauseconesareborne
forphenological
purposes. ofan exceptional
and developmental
September1991]
TOMLINSON ET AL. -POLLINATION
IN PODOCARPACEAE
1291
at the marginsof phyllocladesand have no dropis resorbed
duringthefollowing
morning.
preferred
orientation
(Fig. 1). Otherwise,
cone It can be sustainedlongerif the shootsare
reorientation
can be pronounced,
themecha- enclosedin a plasticbag, as describedunder
nism dependingon whetherthe cone is ter- Materialsand Methods.Figure17 showsthe
minalor lateralon a vegetative
shoot.In Mi- beginning
of drop secretionat 9 p.m.; other
crocachrys
(Fig. 2), terminal
conesare erected illustrations
are ofdropsphotographed
in the
bygrowth
at thebase oftheconeaxis.In Da- morningfollowing
dropsecretion.The pollicrydium
cupressinum
(Fig. 3), theconesoccur nationdropin all taxaexceptPhyllocladus
inat the ends of usuallyshortvegetativeaxes, volvessecretionof thedropontosome adjaand theupturning
of theshoottipis thefirst centwettablesurfacein sucha waythatwhile
evidencethatallowsreproductive
axes to be retaining
contactwiththemicropylar
orifice,
distinguished
fromvegetativeaxes. In other the drop picks up wind-bornepollen either
Dacrydiumspecieswithrobustaxes thiscur- directly
from
or,moreimportantly,
indirectly
vatureis notpossibleand coneorientation
de- wettableareaswherepollenmayalreadyhave
pends on the orthotropy
of the whole shoot beendeposited(e.g.,Zone X in Fig. 11).Non(e.g.,Fig.35). In mostothertaxaconeerection wettableand wettableareasare distinguished
occursjust as thecone expands,as in Dacry- chieflyby the presenceor absenceof white,
carpus(Fig.4) andLagarostrobos
colensoi(Fig. waxysurfacedeposits.Wax maycoverinner
5). In somePrumnopitys
species(e.g.,P. tax- and outersurfaces
oftheepimatiumand even
ifolia,Fig. 6)the candlelikeerectionofyoung theoutersurfaceofthemicropyle,
wherethis
elongatedcones is pronouncedbecause they protrudes.In some Prumnopitys
speciesthe
are lateraland contrastwiththedarkfoliage. wettableregionis structurally
specializedas a
Curvatureis herepossiblewithinthe whole "gutter,"
with
raised
as
describedlatmargins
coneaxis,as demonstrated
experimentally
by er. In all taxa withinvertedovulesand erect
Doyle (1945), who producedS-shapedcones
cones,oncethesecreted
drophasmadecontact
byreorientating
branches.
with
the
adjacent
wettable
surfaceand adheres
In Podocarpus,thecones are lateralat the
to
it
it
by
capillarity,
spreads
downwardby
baseofthenewshootsandsubtended
byeither gravity,
but
retains
contact
with
the
micropylar
bud.scalesor proximalfoliageleaves. Orienorifice
of
(e.g.,
Fig.
9).
The
extent
thedrop's
tationis theresultofthecurvature
ofthelonger
its
spread
is
determined
by
volume
and the
(e.g.,P. totara)orshorter
(e.g.,P. nivalis)naked
of
in
the
it
is
most
extended
topography
cone;
portionoftheconeaxis("peduncle").The exwiththegrooved,guttentof curvature
dependson the orientation speciesofPrumnopitys
terlikeaxis. Pollencan eitherarriveafterthe
oftheparentbranch(cf.Figs.7, 8).
The overallnegativegeotropism,
whatever dropis secreted,or arrivebeforeand adhere
itsmechanism,
inerectconesandovules to thewettablesurface.Capturedgrainsfloat
results
withthe micropyledirecteddownward(Fig. upwardin thedropand becomeconcentrated
orifice.Withdryingor re9). This orientation
is necessaryforthepolli- at the micropylar
nationmechanismto work,and in Figs. 12- sorptionof thedropthepollenis drawninto
and comesto restin thepollen
37 cones and ovules are illustrated
in their themicropyle
chamberon thenucellus.Pollinatedconescan
naturalposition.
be identified
by dissection,because accumu-In the13 taxalist- latedpollencan be observedmicroscopically.
Pollinationmechanism
by reed positively
in Table 1,a pollination
drophas Pollinatedconesalso can be identified
been observedin speciesof the generaDac- versingtheprocess,i.e., if a dropof wateris
regionand theovule
rycarpus,Halocarpus,Lagarostrobos,Lepi- added to themicropylar
erected
the
cone
by
turning
upsidedown,exdothamnus,
PoMicrocachrys,
Phyllocladus,
Conesat thetime istingpollenfloatsout ofthepollenchamber
docarpus,and Prumnopitys.
of drop secretionare illustrated
in Figs. 12- providednoairbubblehasbeentrapped.Reintheovulecausesthenormalprocessof
20. In all taxaexceptPhyllocladus
a common verting
mechanismis shownand may be described pollen flotationto be repeated.This simple
demonstrates
thedependenceof
beforedetailsare presentedforin- manipulation
generally
dividualtaxa. The mechanismin principleis themechanismon pollenbuoyancy.
is exceptional
-becausethedrop
shownin Fig. 11. The mechanismin Phyllo- Phyllocladus
cladus(andprobably
is thesame mechanismconformsto thatgeneralforcoMicrostrobus)
i.e.,thepollination
dropis secretedand
as generalizedforgymnosperms
witha polli- nifers,
withoutcontacting
nationdropas in mostotherfamilies(Fig. 10). retainedbythemicropyle,
The beginning
ofdropsecretion
usuallyoc- any adjacentsurface(Figs. 1, 10). This concursin thelate evening(9-10 p.m.),and the ditionis correlatedwiththe absenceof any
1292
AMERICAN JOURNAL OF BOTANY
[Vol. 78
inPodocarpaceae;
Figs.1-6. Coneorientation
conesterminal
onvegetative
shootsin2-5,lateralin6. 1.Phyllocladus
= pollination
var.alpinus,shootwithyoungovulateconeson phylloclade
arrowheads
margins,
drops.
aspleniifolius
2. Microcachrys
ovulatecone at timeofpollination,
on vegetative
tetragona,
terminal
shootand erectedbyunequal
ofbaseofconeaxis.3. Dacrydium
growth
cupressinum,
veryyoungovulatecone,erectedbycurvature
ofdistalportion
of supporting
axis. 4. Dacrycarpus
ovulateconesat timeof pollination,
each erectedby curvature
of
dacrydioides,
axis.5. Lagarostrobos
erectedbycurvature
ofsterileportion
supporting
colensoi,ovulateconesat timeofpollination,
ofconeaxis.6. Prumnopitys
ovulatecones,lateralon previousyear'svegetative
shoot,eachshowing
a strong
taxifolia,
negatively
geotropic
response.Bars= 1 mmin Figs. 1, 2, 3, 5, and 1 cm in Figs.4, 6.
September 1991]
TOMLINSON ET AL. -POLLINATION
IN PODOCARPACEAE
1293
togravwithrespect
coneorientation
preferred
ityand theabsenceofan epimatium.
7a
1$
9
12-20 document
Cone structure-Figures
at thetime
detailsofovulateconemorphology
of pollinationin some ofthetaxa in whicha
pollinationdrop has been observed.Figures
detailsfora similar
21-30 show structural
andsectional
bothsurface
range,incorporating
viewsofwholeconesand singleovulatecomplexes.Figures31-37 showsimilardetailsin
taxa in whicha pollinationdrophas not yet
been observed,butin whichthecone configthatit is likelyto occur.The
urationsuggests
conesofpodocarpsare minuteat thetimeof
pollination,usuallyof the orderof 3-5 mm
arranged
long.Theyincludea seriesofspirally
bracts,one or more of whichis fertile,
i.e.,
Microcachrys
subtendsan ovulatestructure.
inwhorls.In taxalike
hasconebractsarranged
(Fig.
(Figs.2, 12),Microstrobus
Microcachrys
(Figs. 1, 23), and especially
31), Phyllocladus
is instructure
Saxegothaea,thereproductive
deed conelikebecause the axis is shortand
severalovules (one per fertilebract)are developed. Otherwise,in manytaxa thereare
onlyone to twoovules,and theunitlittleresemblesa cone.
A diagnosticfeatureforthe familyis the
presenceofa singleovuleassociatedwitheach
fertilebract.In mostpodocarpsthe ovule is
in itspollinating
positionby
further
supported
the
a partlyor whollyenvelopingstructure,
epimatium,an appendageof uncertainhomology(denselystippledin Figs.21-37). Furin almostall ofthesespecializedexthermore,
in itsorientation
amples,theovuleis inverted
so thatthe micropyleis directedtowardthe
cone axis (cf. Fig. 11). In mostgenerawith
ovulestheconeaxisalwaysgrowserect
inverted
as wellas
so thattheovuleis topographically
inverted.One exceptionis
morphologically
(Tasmania),whichhas
Lagarostrobosfranklinii
erectovules but invertedcones, so thatthe
orientation
as othergenera
same topographic
the
is achieved(Fig. 32). In Lepidothamnus
Figs. 7-9. Pollinationdrops in Podocarpusnivalis;
ovulateconesare lateralat thebase of thenewseason's
of base of cone axis,
growthand erectedby curvature
(Fig.7) orvershootis horizontal
thesupporting
whether
tical(Fig.8). 7. Conewithtwoovules,thetwopollination
8. Eachconewitha singleovule;
dropsfused(arrowhead).
= pollination
arrowheads
drop.9. Detailofconewithsingle
downthesubtending
dropextended
ovule,thepollination
cone axis; b = bract,e = epimatium,m = micropyle,pd
= pollination
offusedbases
consisting
drop,r= receptacle,
oftwobracts(cf.Figs.24, 25). Bars= 1 mm.
1294
AMERICAN JOURNAL OF BOTANY
__L_----
_J_-- -----
Zone X
.....
Pollinationdrop- -extended
in space
extended
in time
---_--
----
Naked
ovu/e
Naked
ovule
(Most gymnosperms)
L
Pollen scavenging
(Podocarpacae)
[Vol. 78
ovuleis obliquelyerectas is evidentwhenthe
seedmatures
(Fig.27). InDacrydium,
theovule
is inverted
atpollination
butmaybecomepartlyerectedduringseed development
(Fig. 34).
Asalreadystated,
preciseovuleorientation
with
respecttogravity
is essentialtothepollination
mechanismin mosttaxa. Exceptionalgenera
thatlackan epimatiumareMicrostrobus
(two
species)and Phyllocladus
(fourspecies);both
thesegenerahaveerectovules,and all species
are alike.
Information
about cone morphology
and
ovule orientation
is summarizedin Table 1.
In themostreducedand presumably
mostderivedcondition,thecone includesa seriesof
sterilebractsand a singlefertile
bract,thesolitaryovulebeingsubterminal
(e.g.,Dacrycarpusdacrydioides,
compFig.30;Decussocarpus
tonfi,
taxoides,Fig. 37;
Fig. 36; Falcatifolium
Parasitaxusustus,Fig. 33; and Prumnopitys
ferruginea,
Fig. 29).
Special mechanisms-Taxavaryin thedetailsoftheprocessaccording
to ovulenumber
and conetopography
as describedin detailfor
individualtaxa.
Figs. 10, 11. Methodsof pollencapturein gymnospermsin chronological
sequencefromabove. 10. Naked
Phyllocladus
spp.-Ovules areerectand inovuleofmostgymnosperms
witha pollination
drop.Prior
in
serted
the
axil
ofthebract(Fig.23),buthave
to secretion
ofa pollination
drop,ovulemayreceiveunorientation
withrespectto gravdirected
andineffective
pollen(smallarrows);
subsequent- no preferred
ly,pollination
an arilis present
dropissecreted
andbecomestrapforpollen. ity.Atthetimeofpollination
The periodof effective
pollencapture(largearrow)can but littledeveloped(cf. Tomlinson,Takaso,
onlybe extendedforthedurationof droppresentation; and Rattenbury,
1989). The pollinationdrop
thedropis resorbed
finally,
and pollenis drawnintothe remainson the
micropyle
(o in Fig. 23) and
pollenchamber.Pollenmayor maynotbe winged.11.
(Fig. 1).
inPodocarpaceae.
Pollenscavenging
Ovulepartly
orwhol- does notcontactadjacentsurfaces
lyenclosedbyepimatium
conereceives
(dotted).At first,
Podocarpus species-Podocarpus (sensu
in
pollen(smallarrows= ineffective
pollen),somefalling
Zone X, adjacentto themicropyle
regiondesignated
of stricto)
is veryuniform
initsconemorphology
theovule,whichis alwaysinverted
or (Figs. 24, 25) and seemingly
(morphologically
also in its pollithepollination
topographically);
subsequently,
dropis se- nationmechanism,
which
is
constantin the
cretedthrough
themicropyle
ontoZone X whereexisting
pollenis pickedup,pollenfloatsintothepollenchamber; fewspeciesthathavebeenobserved.The polthedropis resorbed
finally,
andmostofthepollenremains linationdrop(Fig. 9) is secretedontotherebractsof
inthepollenchamber.
Thepollination
period(largearrow) ceptacleformedby thetwo inflated
is extendedbothin time(pollenmaybe functional
that thecone,one or bothofwhichmaybe fertile
fallson thecone beforethedropis secreted)and space (Figs. 7, 8, 24, 25). The amountof secreted
thesizeofthetarget),
(ZoneX increases
i.e.,thereis pollen fluidis sufficiently
copiousthatitcanrundown
scavenging.
thegroovebetween
thetwobracts.Wherethere
aretwoovulestheseparatedropsusuallycombine(Figs.7, 8).
tetragona.
13. Halocarpus
12. Microcachrys
Figs. 12-20. Ovulateconesin Podocarpaceaeat timeofpollination.
17. Lagarostrobos
16. Lepidothamnus
laxifolius.
intermedius.
15. Lepidothamnus
dacrydioides.
kirkii.14. Dacrycarpus
19.
(cf.Fig. 5). 18. Prumnopitys
ferruginea.
of dropsecretion
cone scale withcommencement
colensoi,singlefertile
colensoi,whole
taxifolia,portionof singlecone withone completeunit(cf.Fig. 6). 20. Lagarostrobos
Prumnopitys
bract;sb = sterilebract;e =
b = fertile
dropsfromtwoseparateovuleshave fused(arrowhead).
cone,pollination
= pollination
dropor itsrecentremains.Bars=
m = micropyle;
r = receptacle;
g = groove;arrowheads
epimatium;
1 mm.
September 1991]
TOMLINSON ET AL. -POLLINATION
.19
IN PODOCARPACEAE
1295
1296
[Vol. 78
AMERICANJOURNALOF BOTANY
g
|
{
:
(
2? j
/
p
\
\
Lagarostrobus,
tc
*-e.@.
colensiSO
..l
\
t
\
*
Microcachrys
teP
PrS
alpinus/
~~~~Phyllocladus
n
....Prumnopitys
ferru.........
I
intermedius
LepidothamfiUS
Prnopt
errus
PrumnOPity
| Halocarpus kirkii
dacrydioides
Dacrycarpus
dropshave beenobserved,
in certainPodocarpaceaewhosepollination
Figs.21-30. Cone and ovulatestructures
colensci.23.
in surface
viewand section;fromcameralucidadrawings.
tetragona.
22. Lagarostrobos
21. Microcachrys
ofice 24. Podocarpustotara.2 Podocarpusnivalis.26.
asplenfoliusvar. alpinus o micropylar
Phyllocladus
30.Dacrycarpus
28.Prumnopitys
andina.29.Prumnopitysferruginea.
intermedius.
27.Lepidothamnus
kirkii.
Hlalocarpus
(except
wherevisible= solidblack.In all figures
= shaded;micropyle
= stippled;
epimatium
Cutsurfaces
dacrydicides.
(stippled)
"gutter"
byX; X developedas an elongated
dropindicated
Fig.23) regionthatreceivesextendedpollination
in Fig.28. Bars= 1 mm.
September 1991]
TOMLINSON ET AL. -POLLINATION
(ii)
1297
IN PODOCARPACEAE
(32)8
Lagarostrobos
franklinil
Microstrobus
..
fitzgeraldii
........
...a .. .I
,
Parasitaxus
ustus
4~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
X
l 91l
Da crydium
tDacrydium
X
cupressinum
..
X
/
7
]araucarioldes
/~~~~~~~~~......
Decusscarpuscmprtoniil
Decussocarpus
comptoni;i
.
...................
.........
/|
. '' .//..-
Falcatifolium taxoidesid
Figs.31-37. Conesand ovulatestructures
in Podocarpaceaewhosepollination
dropshavenotyetbeenobserved.
ovuleis morphologically
31. Microstrobusfitzgeraldii.
32. Lagarostrobos
erect,butconeis pendulous.33.
franklinii,
37. Fal36. Decussocarpus
Parasitaxusustus.34. Dacrydium
35. Dacrydium
comptonii.
araucarioides.
cupressinum.
taxoides,shadingconventions
as in Figs.21-30. Bars= 1 mm.
cati~folium
1298
AMERICAN JOURNAL OF BOTANY
[Vol. 78
Microcachrys-Ovules
are inserteddistally bractsare fertile,
bractbeingadnate
thefertile
on the bract(Fig. 21); the pollinationdrop, to the epimatium(Fig. 30). The pollination
adheresto theadaxialsurfaceofthe dropis secretedontothesurfaceofthereceptherefore,
bractbase(Fig.12).Underartificial
conditions, tacle,its spreadpossiblybeingfacilitated
by
dropsmaypersistforseveraldays.
thepapillae(Fig. 14). Contrastbetweenwhite,
wettawaxy,nonwettable
andgreen,nonwaxy,
Lagarostrobos
colensoi-Cones areterminal ble surfacesis pronounced.
on thevegetative
shoots(Fig.5) withtheovule
distalon the shortbract(Fig. 22). The drop
Prumnopitys
andina and P. taxifolia-The
originatesfromthe micropyle(Fig. 17) and coneshavean elongated
axis(up to 3 cmlong),
extendsover theadaxial surfaceof thebract withnumerous(up to 12) widelyseparated
ontothecone axis,accumulating
in thebract ovules,each subtendedby one ofthespirally
axil;dropsfromadjacentovulesmayfuse(Fig. arranged
bracts(Fig.6). The mouthofthemi20). Furtherspreadis prevented
primarily
by cropyleis applieddirectly
to a shallow,wettabase
nonwettable
waxydeposits.
blegroove,whichrepresents
thedecurrent
of the bractinsertionand contrastswiththe
surfaces
(Fig.19).
remaining
Halocarpus kirkii
-This resemblesLaga- waxy,nonwettable
raisedso
rostrobos
colensoibutwiththeconecondensed The marginofthegrooveis slightly
and morerobust(Fig. 26). The fertilebracts thata veritable"gutter"is formed(Fig. 28).
are less divergent
so thatthedrophas a nar- Pollen is readilyobservedwithinthe gutter,
rowermeniscusand extendsfarther
downthe bothpriorand subsequentto thesecretionof
the drop.The accumulationof excesspollen
cone axis (Fig. 13).
in the micropylar
regionof the grooveafter
thatpollenscavengLepidothamnusspp.-In Lepidothamnus dropabsorptionsuggests
theconesareterminal
onleafyshoots, ingis effective.
laxifolius
thecone axis is condensed,and limitedreori-Cones are borne
ferruginea
entationis primarily
theresultofgeneralized Prumnopitys
growth
curvature
ofthefertile
shoot.A series laterallytowardthe base of previousyear
winthroughout
oftwoorthreepenultimate
sterilebractsforms shoots.Theycontinuegrowth
a palisadethatcreatesa shallowopen recep- terso thata longaxis witha seriesof sterile
fleshybractsis produced.At the
tacle intowhichthe drop extendsand is re- overlapping
tainedbycapillarity
(Fig. 16).A diagnostic
fea- timeofpollinationthedistalpartoftheaxis,
ture of the genus is the hooked micropyle whichbearsa seriesofmoredelicatespreading
in theseed)and theobliquelyerect sterilebracts,elongatesand becomesoriented
(persistent
The ultimatetwoor fourbractsare
oftheovule(cf.L. intermedius,
orientation
Fig. vertically.
white,waxy,and non27). Underthesecircumstances
capturedpol- narrow,cylindrical,
len travelsinitiallyupwardinto the down- wettable(Fig. 18). Usuallyonlythe ultimate
pobract,in a pseudoterminal
wardlydirectedmicropylar
orifice.It is then or penultimate
drawnintothepollenchamberin thereverse sition,is fertile(Fig. 29). The bractremains
The pollination
dropis
direction
as thedropeitherdries freeoftheepimatium.
bycapillarity
coneaxis
or is resorbed.The U-shapedpassagecan be secretedontothesomewhatinflated
over the whole
reversed
andrepeated
thecone. and can spread extensively
byreorientating
Here,then,thereis an outerpollenreceptacle, wettablesurface(Fig. 18).
as wellas a pollenchamber.Lepidothamnus
is distinctin thatthepollination OtherPodocarpaceae-Othertaxa with a
intermedius
to thegeneralized
thatconforms
sealed because construction
receptacleis morecompletely
insuitableforpollenscavenging
thehookedmicropyle
seemsconsistently
tobe arrangement
lodgedunderthe tip of the opposingsterile clude Acmopyle,Decussocarpus,Falcatifolibract(Figs. 15, 27).
um,and Parasitaxus.We have observedthe
lastthreeclose to,butnotat,thetimeofpolaretwoor linationand havenotyetrecordedpollination
Dacrycarpus
dacrydioides-There
threebracts,fusedbasallyto forma fleshy
pa- dropson them.However,theclose similarity
thesame mechsuggests
pillatereceptacle(Fig. 14). The receptacle
en- in ovule orientation
largesand colorsabruptly
at thetimeof seed anism.Theseand othertaxamaybe discussed
(Figs.32-37).
dispersal.The distalpartof thebractis rep- individually
resentedby a small waxyprotuberance,
developedveryearlyin conedifferentiation,
the
Lagarostrobos
franklini-Cones are termishoots,butpendulousat the
receptacleitselfappearinglaterin association nal on vegetative
withovuleinitiation.
One (lesscommonly
two) timeofpollination
personalcom(A. Shapcott,
September 19911
TOMLINSON ET AL. -POLLINATION
IN PODOCARPACEAE
1299
the developingseeds are
enclosingstructure,
invariousways.Brown'spoint
indeedprotected
onlyat the
emphasizedthatin gymnosperms
does pollenhavedirectactimeofpollination
or "enclosed
cess to theovules.Angiosperms
have theirovules
seededplants,"in contrast,
enclosedin a carpel,a structure
consistently
directaccessofpollentotheovules,
preventing
surfaceforpollenrecepParasitaxusustus-Cones are terminalon butwitha stigmatic
ingymofpollination
erectvegetative
branchesand includea single tion.Relativeefficiency
ovuleintheaxiloftheultimate nospermsand angiospermsmust be underpseudoterminal
orpenultimate
bract(Fig.33). The micropylar stoodin theseterms.
in conifersis bywindbutis
Pollentransfer
orificeis appliedto thecone axis,suitablefor
becauseit requireslarge
evidentlyinefficient
pollenscavenging.
amountsof pollento be dispersedrandomly
theefficiency
Increasing
Dacrydium
spp.-This genusremainsprob- to a verysmalltarget.
selectively
theconesare ter- ofpollencapturemaybe considered
lematic.In D. cupressinum
buthas beenlittleexaminedin
shoots(Fig. 3). advantageous,
minalon upturnedvegetative
Polas a biologicalmechanism.
(Fig.34), gymnosperms
The usuallysolitary
ovuleis inverted
by
butwe have notobserveda pollinationdrop. len capturein conifersmay be facilitated
ofconeconstruction
(Niklas,
In D. araucarioides,
dif- theaerodynamics
conesare indistinctly
fromvegetative
budssincethenu- 1984), but this simplyconcentratespollen
ferentiated
In manygymofthetarget.
merousoverlappingouterbractsare not di- withinthevicinity
thesize of the
as in mostconifers,
vergentand the cone axis does not elongate nosperms,
(Fig.35). One ortwoovulesoccupythecentral ultimatesiteforpollenreceptionis increased
whichexudes
ofa dropoffluid,
cavitysurroundedby the palisade of sterile bythesecretion
and remainsforsomepebracts.Ovulesare invertedand subtendedby fromthemicropyle
occur
how riodoftime(Fig. 10).Othermechanisms
a largebract.It is difficult
to understand
whicharecom- and are clearlyderivedwithinthe gymnopollenreachesthesestructures,
pletely
enclosed.Morefieldworkonthiswidely sperms(Doyle, 1945). However,ifwe accept
theclaimofRothwell(1977) fortheexistence
distributed
genusis required.
of pollinationdropsin fossilovules of Carthenthepollination
gymnosperms,
-Cones arelateral boniferous
Decussocarpus
comptonii
in moderngroups.
on previousseason'svegetative
shoots,witha dropis an ancestralfeature
that
ona mechanism
centers
therefore,
ovule (Fig. 36). Bractand Interest,
singlesubterminal
ofpollinationand
mayincreasetheefficiency
epimatiumare free.
ofthereproductive
biology
be a majorfeature
Falcatifoliumtaxoides-There is a single of Podocarpaceae.The relativelyfewpodonot suitedto
theepimatium, carpswitha cone morphology
subterminal
ovulesurrounding
Phyllocladus,
usuallywiththetipofa sterilebractopposed the mechanism(Microstrobos,
as eitheranfacestheupper Saxegothaea)maybe interpreted
(Fig. 37). Againthemicropyle
cestralor derived.Saxegothaeais clearlydepartofthecone axis.
peculiarrived,becauseofitsmanystructural
and
the
pollen
drop,
it
lacks
a
pollination
ities;
DISCUSSION
awayfromtheovule(Noren,1908;
germinates
RobertBrown(1827) distinguished
gym- Doyle and O'Leary,1935; Loobyand Doyle,
thesituation
mostprecisely
on 1939).It parallels,in thisrespect,
nosperms
fromangiosperms
thebasisofthemechanism
ofpollenreception. ina numberofPinaceaethatlacka pollination
He pointedoutthatingymnosperms
theovule drop(Doyle,1945;Owensand Molder,1975),
in thegenusHesperopeuce
(=
thatis, thepollen moststrikingly
receivesthepollendirectly;
orificeof Tsuga mertensiana;Page, 1989). This simimustbe capturedbythemicropylar
the larityamongthetwofamiliesis assumedto be
theovule(cf.Fig. 10),butin angiosperms
lines.
betweendistinctphyletic
pollenis receivedby thestigmaof theovary a convergence
knownfor
and gametesare deliveredto the ovule by a On theotherhand,the-mechanism
and presumedforMicrostrobus,
but Phyllocladus,
is functional,
pollentube.The distinction
intostructural
termssince seemsancestralwithinthefamilysinceitcoris usuallytranslated
or "naked seeded plants"are respondsto the typegeneralizedwithinthe
gymnosperms
characterizing
(and apparently
definedbytheir"naked"ovules.However,al- gymnosperms
specialized the familiesCephalotaxaceae,Cupressaceae,
thoughtheylack anyconsistently
munication).
UnlikeL. colensoi,theovule is
morphologically
erectand witha lesswell-deonlythebase
velopedepimatium
thatencircles
of the ovule (Fig. 32). Under thesecircumstancestheovule is topographically
inverted
and the pollen-scavenging
mechanismseems
possible.
1300
AMERICAN JOURNAL OF BOTANY
[Vol. 78
at thetimeof
Taxaceae,and Taxodiaceaein theirentirety).bractsand withthemorphology
intimeofthepollencapturepro- pollinationrelatedto the"pollenscavenging"
Anextension
specess is knownforPicea and Pinus.Here the process.Commonlythereis a relatively
ovule is providedwitha pair of micropylar cialized area (Fig. 11, Zone X) adapted for
armsthatsecreteminute"droplets,"
rendering receptionof pollenand thepollinationdrop.
and Microthearmsviscous.Pollencan adhereto these The aberrantgeneraPhyllocladus
schemeas
areplacedinthistraditional
armsand be pickedup subsequently
whenthe strobus
inPhyllocladus
theepimatium
normalpollendrop,secretedby thenucellus, derivedentities,
is produced.Effectively
thisextendstheperiod beinghomologizedwiththearillatestructure
(Tomlinofpollenreceptionbytheovule,as discussed thatdevelopslatein cone ontogeny
1989),unlikethe
by Owens,Simpson,and Molder(1987) and son,Takaso,andRattenbury,
to
whichis a necessaryprecursor
constitutes
a minimalkindofpollenscaveng- epimatium,
data).
ing.
unpublished
(Tomlinson,
ovuleinitiation
If one acceptsthiscomparativeinterpreta-The simplestcondition,thatof Microstrobus
ofthemajority (Fig. 31), is thenconsideredto be totallydetion,thentheconemorphology
invokes
Theoverallpicture
of podocarpspossessinginvertedovulesrep- rivedbyreduction.
thearil
lossoftheepimatium,
resentsa derivedconditionspecializedin re- theevolutionary
beingitsvestige.Clearly,this
lationtoa processthatrenders
pollination
more in Phyllocladus
of the
raisesthequestion picturedependson an interpretation
efficient.
Thisimmediately
termsand is
solelyinconventional
ofthemorphological
natureoftheepimatium, epimatium
whichis absentfromMicrostrobus
and Phyl- supportedby vascularanalysisand comparaofmaturecones(Stiles,1912;
locladus,sincethereis sucha closecorrelation tivemorphology
betweenthepresenceofan epimatium
and the Sinnott,1913; Wilde, 1944). Florin (1951,
thisview intohis genersecretion
ofa pollination
drop.In theconven- 1954) incorporated
inconifers
but
tionalview generatedby Sinnott(1913) and alizedpictureofconereduction
acceptedby subsequentauthors(e.g.,Wilde, made no newobservations.
oftheepi1944; Florin,1954),partforpartcomparison In biologicalterms,thefunction
of the axillaryfertilecomplexof the ovulate matiumhasbeenlittlediscussed.Thestructure
of
rolein thedevelopment
conesof Pinaceaeand Podocarpaceaeis pos- has no consistent
the dissemithatcharacterizes
sible(Fig. 38). In Pinaceae,thereis a pair of the fleshiness
ovulesinsertedbasallyand withinverseori- nulesandis essentialtotheirdispersal.A fleshy
ofways
canbe producedina diversity
entationon a scale (theovuliferous
scale) in structure
theaxil of each fertile
bract.The ovuliferous (Fig. 38, lowerleft).For example,in Dacrybythebase
is formed
receptacle
scale itselfis homologizedwiththe reduced carpusa fleshy
branchaxisfoundinsomepresumed
ancestors ofthebractsbeneaththeseed,thedistalpart
transitional
(theCordaitalesandextinct
groups of the fertilebractbeingadnate to the epiofconifers).
matium,whichis not fleshy.Podocarpusis
Thispaleobotanical
evidencewasassembled somewhatsimilar,butthebractis notadnate.
studiesofFlorin In Dacrydiumtheepimatiumenvelopesonly
bytheextensivecomparative
exposed
(e.g., 1951, 1954). The singleovule of podo- thebaseoftheseed,whichis otherwise
theepimatiumbecarpshas,forthemostpart,thesameinverted (Fig. 34). In Prumnopitys
thebract
structure,
fleshy
orientation
as in Pinaceae,and thepresumed comestheattractive
(Fig. 38). In taxa like
unelaborated
homolo- remaining
ovuliferousscale is conventionally
whichis reltheepimatium,
whichoftenencloses Lepidothamnus,
gizedwiththeepimatium,
theovule to greateror lesserextent.Support ativelyconspicuousat thetimeofpollination,
in thematuenlargement
forthehomologyofepimatiumwiththeovu- showslittlefurther
liferousscale comes fromcomparativeanat- rationoftheseed (Fig. 27), thebasal portion
the
have a vascularsupply of thecone axis becomesred and fleshy,
omy.Both structures
black.These
in whichxylemand phloemhave an inverted seed coatbecominga contrasted
orientation
(Fig. 38), i.e., withxylemabaxial fewexamplesillustratethe divergentdevelduringseedmaturation,
ratherthanadaxial (Sinnott,1913). The sim- opmentalpossibilities
plest(butnotnecessarily
ancestral)condition involvingvariouspartsof thesehighlyspeparticiis thenrepresented
by taxa likeMicrocachryscializedconesand withoutconsistent
and Saxegothaea,witha moreobviouscone- pationoftheepimatium.
An alternative
to theidea thatevolutionin
likeorganization,
sinceeach cone has several
ofpodocarpshas proceeded
fertilebracts.Saxegothaeais, however,spe- conemorphology
loss of the
In most by specializationand ultimately
cializedin itspollinationmechanism.
cone can be based on the polliotherpodocarps,theseedconesarehighly
spe- ovuliferous
the
withonlyoneortwofertile nationmechanism.In thisinterpretation,
cialized,commonly
September19911
TOMLINSON ET AL. -POLLINATION
PINACEAE
()
1301
IN PODOCARPACEAE
lPODOCARPACEAE
epimatium
ovule
~~~~~~~~~~bract
bract
m
-
1
ep_m
.
phloem
_
SAXEGOTHAEA
2r
0
(n
Cn
mepimatium
eOOA pimoatiumi
MOST
PODOCARPS
j
-I
F
ic
atum
bract
fDISSEMINULE
lW
zS
\\
'
~~~~~~~~receptacle||l
X
RUMNOPITYS
ZONE X
ovule
aril
MICROCACHRYS
rn
recepta
no receptacle
~~~~ovule LEPIDOTHAMUS
I:
receptacle
9
PHYLLOCLADUS
MICROSTROBUS
Fig. 38. Evolutionarymorphologyof the podocarpaceous cone. Pinaceae: the conventionalinterpretationof the
with
ovuliferousscale as a branch homologue withinvertedvascular bundles. Podocarpaceae: the same configuration
the ovuliferousscale an epimatium,as in Microcachrysand Saxegothaea. The arrangementin most podocarps with
one to two ovules per cone and the pollinationmechanismdescribedhere may be derived fromthe conditionin these
two genera.Phyllocladusand Microstrobosthenrepresentthe ultimatereduction,withthe epimatiumreducedto a latedevelopingaril (Phyllocladus);or whollyabsent (Microstrobus).This implies loss of the epimatiumas an evolutionary
trend(arrow,right).In the developmentof the seed (S) into a fleshydispersalunitin othergenera,the epimatiummay
variouslyor may not contributeto the disseminule (fruitanalogue) as illustratedby Dacrycarpus,Prumnopitys,and
Lepidothamnus.However, the situationcan be reversedand the epimatium derived de novo (arrow far right),if the
progressivespecialization of the pollinationmechanism is considered,as we hypothesize.
e.g., Ullmannia(Stewart,
conifers,
epimatium
hasarisende novoanditrepresents transition
developmentalevidence
a structure
intimately
associatedwiththepol- 1983). Preliminary
len scavengingprocess.An ancestryforthe shows that the epimatiumalways precedes
in sucha waythatit produces
Podocarpaceaewithina groupthatmayhave ovuleinitiation
an essentialinovuleorientation,
lackedan ovuliferous
scalemaynotbe difficulttheinverted
mechanism.
ofthepollenscavenging
to postulate,sincetheconditionoccursin the gredient
1302
AMERICAN JOURNAL OF BOTANY
[Vol. 78
One mustemphasizethatovules in gymno- cialized mechanismsin theirpollinationbidetailedexamand have no ologyshowsthattheirfurther
spermsare alwaysorthotropous
benefit,
(unlike inationcan be pursuedwithscientific
mechanismforreorientation
inherent
emphasishasbeenput
doubleinteg- especiallyas increasing
withtheirfrequent
angiosperms
forcefor
as theadaptivedriving
forcurvature). on pollination
capability
umentsand inherent
oftheseed habit
may have theoriginand specialization
Epimatiumand outerintegument
butthisis not (Haigand Westoby,1989).However,one canequivalentbiologicalproperties,
to implythattheyare homologues.The con- notdisassociateoneaspectofthereproductive
feature
scenariopresentedin processfromanother.A characteristic
ventionalevolutionary
composed
withMicrostrobusofmostpodocarpsis a disseminule
Fig.38 thuscanbe reversed,
brightly
beingthe antecedenttypes, of a largeseed and associatedfleshy,
and Phyllocladus
withanimal
and correlated
in theirerectovulesand simplepol- coloredstructures
reflected
unitseems
Selectionforthisdispersal
linationmechanism.The arilofPhyllocladus dispersal.
ofovulenumberper
towardreduction
fortheepimatium directed
couldthenbe theprecursor
featureof cone. A typologicalreductionseries exists
thathas becomethe characteristic
mostpodocarps,but as a derivedand not an withinthefamily;thismaymirrortheinterseed
efficiency,
pollination
between
franklinii dependence
Lagarostrobos
ancestralstructure.
couldfitintothispicturesinceovuleinversion biology,and cone morphology.Podocarps
properdemographic
clearlyhave distinctive
by cone inversion(Fig. 32).
is determined
andbiologyof ties(Ogden,1985)as wellas unusualseedand
Otheraspectsofthestructure
sce- seedlingstrategies(Philipson and Molloy,
podocarpscomplicatebothevolutionary
dependenton highlydenarios.Pollenin mostpodocarpsis saccate,or 1990),all ultimately
fieldwork
Continued
winged(Tegner,1965; Pocknall,1981), i.e., rivedconemorphologies.
ofthe on the familyshouldbe pursued,because it
extensions
withtwoorthreebladderlike
and relationships
exine(as in thefamiliartextbookillustrationswill clarifythe systematics
group
southern
andimportant
of Pinus). Doyle (1945) suggestedthatthese ofthisdistinctive
pollen ofplants.
wereessentialformaintaining
structures
in thepollendrop,butnotin air.He
buoyancy
betweenthepresence
noteda closecorrelation
LITERATURE CITED
ofwingedpollenand a pollinationdropin Pinaceae. A similarsituationmayexistin Po- BROWN,R. 1827. Characterand descriptionof Kingia;
a new genus of plants found on the south-westcoast
docarpaceae;Saxegothaealacks wingedpolof New Holland. With observationson the structure
thewingscanbe described
len.In Phyllocladus
ovulum,and on thefemaleflower
ofitsunimpregnated
onlyas vestigial.Dacrydiumlacks wingsfor
ofCycadeae and Coniferae.Reprintedfromnarrative
to Tegner(1965),but
themostpart,according
of a surveyof the intertropicaland WesternCoasts
of Australia performedbetween the years 1818 and
accordingto Pocknall
not D. cupressinum,
1822, Captain Philip P. King R.N., F.R.S., F.L.S., vol.
reexdeserves
situation
the
Clearly
(1981).
2. London.
aminationin thefamilyas a whole.A furtherDE LAUBENFEIS,
D. J. 1972. Flore de la Nouvelle Cabiological mechanismproposed by Doyle
l6donie et Dependances vol. 4. Gymnospermes.Mua pre(1945) was thatpollenwingsguaranteed
seum National d'histoirenaturelle,Paris.
ofthepollenon thenucellus
ferred
orientation
1988. Coniferalesin Flora Malesiana, series 1,
vol. 10 (3). MartinusNijhoff.The Hague.
Obin orderto facilitate
pollengermination.
servations
by Lill and Sweet(1977) on Pinus DOYLE, J. 1945. Developmental lines in pollinating
mechanismsin the Coniferales.ScientificProceedings
radiatado notsupportthisidea.
oftheRoyal Dublin SocietySeries A 24: 43-62 (New
in
bithese
be
a
key
genus
may
Dacrydium
series).
It apparentlylacks
ological interpretations.
, AN M. O'LEARY. 1935. Pollination in Saxeseempollenwings,has a cone morphology,
gothaea. ScientificProceedings of the Royal Dublin
Society21: 175-179.
inglywithtotallyenclosedovules,and no polThe pre- EAMES, A. J. 1913. The morphologyofAgathisaustralis.
linationdrophas yetbeen reported.
Annals of Botany (London) 27: 1-38.
shouldbe FLowN,
natureofourobservations
liminary
R. 1951. Evolution in cordaites and conifers.
clearfromthisdiscussion,butpointstheway
Acta Horti Bergiana 15: 285-388.
necessaryfieldworkand directobto fiurther
1954. The femalereproductiveorgansofconifers
and taxads. Biological Reviews29: 367-389.
servationofthemechanism.
The Podocarpaceae, with an intriguing HAIG, D., AND M. WESTOBY. 1989. Selective forcesin
the emergenceof the seed habit. Biological Journalof
havebeenrelative"Gondwana"distribution,
theLinnean Societyof London 38: 215-238.
andtheroletheyplay HAmmNS,
bybotanists,
lyneglected
R. J., N. PRAKASH, AND D. J. NIKLEs. 1984.
processesin coevolutionary
in interpreting
Pollination in Araucaria Juss. AustralianJournal of
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