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Pollination Drop in Relation to Cone Morphology in : 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 . Accessed: 23/08/2011 15:47

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http://www.jstor.org AmericanJournal of Botany 78(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 2HarvardForest, Petersham, Massachusetts 01366; and 3Departmentof Botany, University of Auckland, Auckland,

Observationof ovulatecones at thetime of pollinationin the southernconiferous family Podocarpaceaedemonstrates a distinctivemethod of pollencapture, involving an extended pollinationdrop. Ovules in all generaof the family are orthotropousand singlewithin the axil of each fertilebract. In Microstrobusand Phyllocladusovules are-erect (i.e., the micropyle directedaway from the cone axis) and are notassociated with an ovule-supportingstructure (epimatium). in thesetwo genera must land directly on thepollination drop in theway usualfor , as observed in .In all othergenera, the ovule is inverted (i.e., the micropyleis directedtoward the cone axis) and supportedby a specializedovule- supportingstructure (epimatium). In Saxegothaeathere is no pollinationdrop and gametesare deliveredto theovule by pollen tube growth. Pollination drops were observed in sevenof the remaininggenera. In thesegenera the drop extends over the adjacent surface or coneaxis and can retainpollen that has arrivedprior to dropsecretion ("pollen scavenging"). The pollen floatsupward into the micropylar cavity. The configurationofthe cone in othergenera in which a pollinationdrop has notyet been observed directly suggests that pollen scavenging is general withinthe family and mayincrease pollination efficiency by extendingpollination in spaceand time.Increased pollination efficiency may relate to thereduction of ovule number in eachcone, oftento one in manygenera, a derivedcondition. A biologicalperspective suggests that animal dispersalof large may be theultimate adaptive driving force that has generatedthe need forgreater pollination efficiency.

We heredocument that the pollination drop fleshyseeds dispersedby animals (mainly mechanismof many members of the southern ). hemisphereconiferous family Podocarpaceae A pollinationdrop is knownto be produced (podocarps)differs from that in most gym- in all speciesof ,Cupressa- nosperms.The dropcan "scavenge"pollen that ceae,, and Taxodiaceae that have been has previouslyfallen near the ovule,prior to studied(Takaso, 1990). In Araucariaceaeno dropsecretion. Presumably this increases the pollinationdrop occurs, the gametes being de- efficiencyof pollinationand is correlatedwith liveredto themicropyle by pollen tube growth thereduced number of ovules per cone in most (Eames, 1913; Haines, Prakash,and Nikles, podocarps.The Podocarpaceae,unlike most 1984). The greatestdiversity in pollination otherconifers, are largelycharacterized by mechanismsis knownfor , in which a pollinationdrop is reportedfor Picea and Pinus,while othergenera have mechanisms 1 Receivedfor publication 21 January1991; revision withoutdrop secretion, such as pollenengulf- accepted7 May 1991. The authorsthank the Directors and ChiefRangers of mentor pollen tube growth (Doyle, 1945). Ab- Mt. TongariroNational Park; AucklandRegional Au- senceof a dropis consideredderived since the thorityBotanical Garden, Manurewa; Waitakere Conser- presenceof a pollinationdrop may be a very vationArea, Auckland; Kauaeranga Reserve, Cor- ancientfeature of gymnosperms (cf. Rothwell, omandel,all in New Zealand;Mt. Field NationalPark, 1977). In Podocarpaceaethere has been no ;and Fairchild Tropical Garden, Miami, Florida in forpermission to collect and makeobservations in several observationof pollination mechanisms nat- protectedareas; Alison Shapcott, University of Tasmania; urallygrowing . Doyle (1945) suggested C. J.Quinn, University ofNew South Wales; J.-M. Veillon, thatthe Podocarpaceae formed a parallelseries CentreO.R.S.T.O.M., Noumea, ; and Ewen to the Pinaceae,also involvingloss of a pol- K. Cameron,University of Aucklandfor further collec- linationdrop, but he describeda pollination tionsand fieldassistance; and EllenMoriarty and Toku- drop onlyin one specieseach of shiroTakaso for help with illustrations. Field work in the SouthPacific was supportedby a grantto PBT fromthe and Prumnopityscultivated in Irishgardens. ResearchCommittee of the National Geographic Society. ,which lacks a pollinationdrop 4Author forcorrespondence. (Noren,1908; Doyle and O'Leary,1935), was 1289 1290 AMERICAN JOURNAL OF BOTANY [Vol. 78

TABLE 1. Podocarpaceae.Taxa withan observedpollination drop

No. fertile Taxon Localityr Ovule orientationb Dacrycarpusdacrydioides (NZ) 1(-2) Inverted kirkii Kelly's Road, Waitemata (NZ) 2-3 Inverted Lagarostroboscolensoi Cult. Auckland Univ. Campus (NZ) 2-3 Inverted Lepidothamnusintermedius Kauaeranga For. Res. (NZ) 1(-2) Obliquely erect Lepidothamnuslaxifolius TongariroNat. Park (NZ) 1(-2) Obliquely erect Microcachrystetragona Mt. Field Nat. Park (T) 8-16 Inverted Phyllocladusaspleniifolius var. alpinus TongariroNat. Park (NZ) 1-5 Erect Phyllocladustrichomanoides Cornwall Park, Auckland (NZ) 2-7 Erect Cult. Fairchild Tropical Garden (US) 1-2 Inverted TongariroNat. Park (NZ) 1-2 Inverted Manurewa Bot. Gard. (NZ) 1-2 Inverted Prumnopitysandina Cult. Hobart Bot. Gard. (T) 5-10 Inverted Prumnopitysferruginea Waitakere Hills (NZ) 1(-2) Inverted Prumnopitystaxifolia Manurewa Bot. Gard. (NZ) 5-10 Inverted a NZ = North Island, New Zealand, T = Tasmania, US = United States. b Morphological orientationwith respectto cone axis. consideredby Doyle to be highlyderived and Most observationswere made on populations analogousto Tsuga.Our observationsgreatly in theAuckland region of New Zealand (Table amplifythe picture for Podocarpaceae and show 1) sincethese provided convenient access to manyunique features of their pollination; per- photomicrographicfacilities. Pollination drops haps onlyin Picea and Pinus,which have an canbe observeddirectly in the field with a hand abilityto retainpollen prior to dropsecretion, lens. Detached shootswith ovulate cones at mayparallels be drawn(Owens, Simpson, and the stageof pollinationwere brought into a Molder,1981; Owens,Simpson, and Caron, shelteredroom, kept in water,and enclosedin 1987). a plasticbag. This usuallyresults in drop se- The Podocarpaceaeincludes 18 genera(17 cretionin a normalway. Pollination drop se- ifPhyllocladus is excludedas Phyllocladaceae; cretionis mostlyin thelate evening,and the Page, 1990) and about 200 speciesof dropsare normallyresorbed by late morning, and trees,with a widedistribution in theGon- but enclosedcut shootscan retaindrops for dwanaregion, i.e., presentday Africa,south- severaldays. In Microcachrystetragona, fresh eastAsia, Australasia, and SouthAmerica (De conesflown from Tasmania to Aucklandper- Laubenfels,1988). New Caledonia (18 spp.) mittedthe photographyof pollinationdrops andNew Zealand (17 spp).both represent local in thisway. Microphotography ofcones at the centersof diversity and endemism. typ- stage of pollinationwas done with a Wild icallyoccupy montane habitats in thetropics, stereomicroscopeusing Ektachromecolor butin New Zealandare a majorcomponent of transparencyfilm (ASA 100);Figs. 1-9, 12-20 themixed podocarp forest at all altitudesand are black-and-whitereproductions from these are frequentlydominant. Recent generic re- transparencies. alignmenthas greatlyclarified the status of cer- Somemanipulation of ovules with and with- taingroups, chiefly by dismembermentof the outcaptured pollen grains was doneunder the largeand previously unnatural genera, Dacryd- microscopeto understandthe mechanicsof iumand Podocarpus (e.g., Tegner, 1967; Quinn, pollenmovement. Reorientation of ovules with 1970,1982, 1987; De Laubenfels,1972, 1988; enclosedpollen demonstrated the buoyancy of Page, 1989, 1990). pollenwithin natural drops, or withindrops simulatedby addingwater. MATERIALS AND METHODS RESULTS Observationswere made on field-growntrees fromwild and cultivatedpopulations in the Generalmechanisms- Cone orientation -An periodSeptember to December1989, in New intrinsicfeature of the pollination mechanism Zealand,Tasmania, and New Caledonia.Rec- of mostpodocarps is the erectorientation of ognitionof thepollination process was facili- thecone at thetime of pollination, commonly tatedby continualmonitoring of shootdevel- broughtabout by growth curvature at the-time opmentin a diversityof podocarps undertaken thecone expands.Phyllocladus is an example forphenological and developmentalpurposes. ofan exceptionalgenus because cones are borne September1991] TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1291

at the marginsof phyllocladesand have no dropis resorbedduring the following morning. preferredorientation (Fig. 1). Otherwise,cone It can be sustainedlonger if the shootsare reorientationcan be pronounced,the mecha- enclosedin a plasticbag, as describedunder nism dependingon whetherthe cone is ter- Materialsand Methods.Figure 17 showsthe minalor lateralon a vegetativeshoot. In Mi- beginningof drop secretionat 9 p.m.; other crocachrys(Fig. 2), terminalcones are erected illustrationsare ofdrops photographed in the bygrowth at thebase ofthe cone axis. In Da- morningfollowing drop secretion.The polli- crydiumcupressinum (Fig. 3), thecones occur nationdrop in all taxaexcept Phyllocladus in- at the ends of usuallyshort vegetative axes, volves secretionof thedrop onto some adja- and theupturning of the shoottip is thefirst centwettable surface in sucha waythat while evidencethat allows reproductive axes to be retainingcontact with the micropylarorifice, distinguishedfrom vegetative axes. In other the drop picks up wind-bornepollen either Dacrydiumspecies with robust axes thiscur- directlyor, more importantly, indirectly from vatureis notpossible and coneorientation de- wettableareas where pollen may already have pends on the orthotropyof the whole beendeposited (e.g., Zone X in Fig. 11). Non- (e.g.,Fig. 35). In mostother taxa cone erection wettableand wettableareas are distinguished occursjust as thecone expands,as in Dacry- chieflyby the presenceor absence of white, carpus(Fig. 4) andLagarostrobos colensoi (Fig. waxysurface deposits. Wax may coverinner 5). In somePrumnopitys (e.g., P. tax- and outersurfaces of the epimatium and even ifolia,Fig. 6)the candlelikeerection of young theouter surface of the micropyle, where this elongatedcones is pronouncedbecause they protrudes.In some Prumnopitysspecies the are lateral-and contrastwith the dark foliage. wettableregion is structurallyspecialized as a Curvatureis here possiblewithin the whole "gutter,"with raised margins as describedlat- cone axis,as demonstratedexperimentally by er. In all taxa with ovules and erect Doyle (1945), who producedS-shaped cones inverted by reorientatingbranches. cones,once the secreted drop has made contact In Podocarpus,the cones are lateralat the withthe adjacent wettable surface and adheres base ofthe new and subtendedby either to it by capillarity,it spreadsdownward by bud.scalesor proximalfoliage . Orien- gravity,but retains contact with the micropylar tationis theresult of the curvature of the longer orifice(e.g., Fig. 9). The extentof the drop's (e.g.,P. totara)or shorter (e.g., P. nivalis)naked spreadis determinedby its volume and the portionof the cone axis ("peduncle").The ex- topographyof the cone; it is mostextended in tentof curvaturedepends on the orientation speciesof with the grooved, gut- ofthe parent branch (cf. Figs. 7, 8). terlikeaxis. Pollencan eitherarrive after the The overallnegative geotropism, whatever dropis secreted,or arrivebefore and adhere itsmechanism, results in erectcones and ovules to thewettable surface. Captured grains float withthe micropyledirected downward (Fig. upwardin thedrop and becomeconcentrated 9). This orientationis necessaryfor the polli- at the micropylarorifice. With drying or re- nationmechanism to work,and in Figs. 12- sorptionof thedrop the pollen is drawninto 37 cones and ovules are illustratedin their themicropyle and comesto restin thepollen naturalposition. chamberon thenucellus. Pollinated cones can be identifiedby dissection,because accumu- Pollinationmechanism -In the 13 taxalist- latedpollen can be observedmicroscopically. ed positivelyin Table 1,a pollinationdrop has Pollinatedcones also can be identifiedby re- been observedin speciesof the generaDac- versingthe process, i.e., if a dropof wateris rycarpus,Halocarpus, , Lepi- added to themicropylar region and theovule dothamnus,, Phyllocladus, Po- erectedby turningthe cone upsidedown, ex- docarpus,and Prumnopitys.Cones at thetime istingpollen floats out of thepollen chamber of drop secretionare illustratedin Figs. 12- providedno airbubble has been trapped. Rein- 20. In all taxa exceptPhyllocladus a common vertingthe ovule causes the normal process of mechanismis shownand may be described pollen flotationto be repeated.This simple generallybefore details are presentedfor in- manipulationdemonstrates the dependence of dividualtaxa. The mechanismin principleis themechanism on pollenbuoyancy. shownin Fig. 11. The mechanismin Phyllo- Phyllocladusis exceptional-because the drop cladus(and probably Microstrobus) is the same mechanismconforms to thatgeneral for co- as generalizedfor gymnosperms with a polli- nifers,i.e., the pollination drop is secretedand nationdrop as in mostother families (Fig. 10). retainedby themicropyle, without contacting The beginningof drop secretion usually oc- any adjacentsurface (Figs. 1, 10). This con- cursin thelate evening(9-10 p.m.), and the ditionis correlatedwith the absence of any 1292 AMERICAN JOURNAL OF BOTANY [Vol. 78

Figs.1-6. Coneorientation in Podocarpaceae; cones terminal on vegetativeshoots in 2-5, lateral in 6. 1. Phyllocladus aspleniifoliusvar. alpinus,shoot with young ovulate cones on phylloclademargins, arrowheads = pollinationdrops. 2. Microcachrystetragona, ovulate cone at timeof pollination,terminal on vegetativeshoot and erectedby unequal growthof base ofcone axis. 3. Dacrydiumcupressinum, very young ovulate cone, erected by curvature of distal portion of supportingaxis. 4. Dacrycarpusdacrydioides, ovulate cones at timeof pollination,each erectedby curvatureof supportingaxis. 5. Lagarostroboscolensoi, ovulate cones at timeof pollination, erected by curvature of sterile portion ofcone axis. 6. Prumnopitystaxifolia, ovulate cones, lateral on previousyear's vegetative shoot, each showing a strong negativelygeotropic 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

preferredcone orientation with respect to grav- ityand theabsence of an epimatium.

Cone structure-Figures12-20 document detailsof ovulate cone morphology at thetime 7a of pollinationin some of thetaxa in whicha pollinationdrop has been observed.Figures 21-30 show structuraldetails for a similar range,incorporating both surface and sectional viewsof whole cones and singleovulate com- plexes.Figures 31-37 showsimilar details in taxa in whicha pollinationdrop has not yet been observed,but in whichthe cone config- 1$ urationsuggests that it is likelyto occur.The cones of podocarpsare minuteat thetime of pollination,usually of the orderof 3-5 mm long.They include a seriesof spirally arranged bracts,one or more of whichis fertile,i.e., subtendsan ovulate structure.Microcachrys has conebracts arranged in whorls.In taxalike Microcachrys(Figs. 2, 12), Microstrobus(Fig. 31), Phyllocladus(Figs. 1, 23), and especially Saxegothaea,the reproductive structure is in- deed conelikebecause the axis is shortand severalovules (one per fertilebract) are de- veloped. Otherwise,in manytaxa thereare onlyone to twoovules, and theunit little re- semblesa cone. A diagnosticfeature for the familyis the presenceof a singleovule associated with each fertilebract. In mostpodocarps the ovule is furthersupported in itspollinating position by a partlyor whollyenveloping structure, the epimatium,an appendageof uncertainho- mology(densely stippled in Figs.21-37). Fur- thermore,in almostall ofthese specialized ex- amples,the ovule is invertedin itsorientation so thatthe micropyleis directedtoward the 9 cone axis (cf. Fig. 11). In most generawith invertedovules the cone axis always grows erect so thatthe ovule is topographicallyas wellas morphologicallyinverted. One exceptionis Lagarostrobosfranklinii(Tasmania), which has erectovules but invertedcones, so thatthe same topographicorientation as othergenera is achieved(Fig. 32). In Lepidothamnusthe

Figs. 7-9. Pollinationdrops in Podocarpusnivalis; ovulatecones are lateralat thebase of thenew season's growthand erectedby curvatureof base of cone axis, whetherthe supporting shoot is horizontal(Fig. 7) or ver- tical(Fig. 8). 7. Conewith two ovules, the two pollination dropsfused (arrowhead). 8. Eachcone with a singleovule; arrowheads= pollinationdrop. 9. Detailof cone with single ovule,the pollination drop extended down the subtending cone axis; b = bract,e = epimatium,m = micropyle,pd = pollinationdrop, r = receptacle,consisting of fused bases oftwo bracts (cf. Figs. 24, 25). Bars= 1 mm. 1294 AMERICAN JOURNAL OF BOTANY [Vol. 78

ovule is obliquelyerect as is evidentwhen the seedmatures (Fig. 27). In ,the ovule is invertedat pollinationbut may become part- ly erectedduring development(Fig. 34). As alreadystated, precise ovule orientation with respectto gravityis essentialto thepollination mechanismin mosttaxa. Exceptionalgenera thatlack an epimatiumare Microstrobus(two Zone X __L_---- _J_------..... species)and Phyllocladus(four species); both thesegenera have erectovules, and all species are alike. Pollinationdrop- -extended Informationabout cone morphologyand extended in space ovule orientationis summarizedin Table 1. in time In themost reduced and presumablymost de- rivedcondition, the cone includesa seriesof sterilebracts and a singlefertile bract, the sol- itaryovule beingsubterminal (e.g., Dacrycar- pusdacrydioides, Fig. 30; Decussocarpuscomp- tonfi,Fig. 36; Falcatifoliumtaxoides, Fig. 37; Parasitaxusustus, Fig. 33; and ,Fig. 29).

---_------Special mechanisms-Taxavary in the de- Pollen scavenging NakedNaked ovuleovu/e L tailsof the process according to ovulenumber (Most gymnosperms) (Podocarpacae) and conetopography as describedin detailfor individualtaxa. Figs. 10, 11. Methodsof pollencapture in gymno- spermsin chronologicalsequence from above. 10. Naked ovuleof most gymnosperms with a pollinationdrop. Prior Phyllocladusspp. -Ovules are erectand in- to secretionof a pollinationdrop, ovule may receive un- sertedin the axil of the bract (Fig. 23), but have directedand ineffectivepollen (small arrows); subsequent- no preferredorientation with respect to grav- ly,pollination drop is secretedand becomes trap for pollen. ity.At thetime of pollination an arilis present The periodof effectivepollen capture (large arrow) can but littledeveloped (cf. Tomlinson,Takaso, onlybe extendedfor the duration of drop presentation; and Rattenbury,1989). The pollinationdrop finally,the drop is resorbedand pollenis drawninto the remainson the in pollenchamber. Pollen may or maynot be winged.11. micropyle(o Fig. 23) and Pollenscavenging in Podocarpaceae.Ovule partly or whol- does notcontact adjacent surfaces (Fig. 1). lyenclosed by epimatium (dotted). At first,cone receives pollen(small arrows = ineffectivepollen), some falling in Podocarpus species-Podocarpus (sensu regiondesignated Zone X, adjacentto themicropyle of stricto)is veryuniform in itscone morphology theovule, which is alwaysinverted (morphologically or (Figs. 24, 25) and seeminglyalso in its polli- topographically);subsequently, the pollination drop is se- nationmechanism, which is constantin the cretedthrough the micropyle onto Zone X whereexisting pollenis pickedup, pollen floats into the pollen chamber; fewspecies that have beenobserved. The pol- finally,the drop is resorbedand most of the pollen remains linationdrop (Fig. 9) is secretedonto the re- inthe pollen chamber. The pollinationperiod (large arrow) ceptacleformed by thetwo inflatedbracts of is extendedboth in time(pollen may be functionalthat thecone, one or bothof whichmay be fertile fallson thecone beforethe drop is secreted)and space (Figs. 7, 8, 24, 25). The amountof secreted (ZoneX increasesthe size of the target), i.e., there is pollen fluidis sufficientlycopious that it can run down scavenging. thegroove between the two bracts. Where there aretwo ovules the separate drops usually com- bine(Figs. 7, 8).

Figs. 12-20. Ovulatecones in Podocarpaceaeat timeof pollination.12. Microcachrystetragona. 13. .14. Dacrycarpusdacrydioides. 15. Lepidothamnusintermedius. 16. Lepidothamnuslaxifolius. 17. Lagarostrobos colensoi,single fertile cone scale withcommencement of dropsecretion (cf. Fig. 5). 18. Prumnopitysferruginea. 19. Prumnopitystaxifolia, portion of singlecone withone completeunit (cf. Fig. 6). 20. Lagarostroboscolensoi, whole cone,pollination drops from two separateovules have fused(arrowhead). b = fertilebract; sb = sterilebract; e = epimatium;m = micropyle;r = receptacle;g = groove;arrowheads = pollinationdrop or itsrecent remains. Bars = 1 mm. September 1991] TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1295

.19 1296 AMERICANJOURNAL OF BOTANY [Vol. 78

g | { : 2 ? j \ \ tc Lagarostrobus, colensiSO

( / p *-e.@. ..l \ t \ * ~~~~/

MicrocachrysteP PrS n

....Prumnopitys ferru...... LepidothamfiUSintermedius I PrumnOPity | Halocarpus kirkii

Prnopt errus dacrydioidesDacrycarpus

Figs.21-30. Cone and ovulatestructures in certainPodocarpaceae whose pollination drops have beenobserved, in surfaceview and section;from camera lucida drawings. 21. Microcachrystetragona. 22. Lagarostroboscolensci. 23. Phyllocladusasplenfolius var. alpinus o micropylarofice 24. Podocarpustotara. 2 Podocarpusnivalis. 26. Hlalocarpuskirkii. 27. intermedius. 28. Prumnopitys andina. 29. Prumnopitysferruginea. 30. dacrydicides.Cut surfaces = stippled;epimatium = shaded;micropyle where visible = solidblack. In all figures(except Fig.23) regionthat receives extended pollination drop indicated by X; X developedas an elongated"gutter" (stippled) in Fig.28. Bars= 1 mm. September 1991] TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1297

(ii) (32)8

Lagarostrobos franklinil Microstrobus .. fitzgeraldii ......

.. ...a .I , ustus

4~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

X Da crydiuml 91l tDacrydium cupressinum X 7 ]araucarioldes

.. X / /~~~~~~~~~......

Decusscarpuscmprtoniil

Decussocarpus comptoni;i...... | . . '' .//..- / Falcatifolium taxoidesid

Figs.31-37. Conesand ovulatestructures in Podocarpaceaewhose pollination drops have not yet been observed. 31. Microstrobusfitzgeraldii.32. Lagarostrobos franklinii, ovule is morphologicallyerect, but cone is pendulous.33. Parasitaxusustus. 34. Dacrydiumcupressinum. 35. Dacrydiumaraucarioides. 36. Decussocarpuscomptonii. 37. Fal- cati~foliumtaxoides, shading conventions as in Figs.21-30. Bars= 1 mm. 1298 AMERICAN JOURNAL OF BOTANY [Vol. 78

Microcachrys-Ovulesare inserteddistally bractsare fertile,the fertile bract being adnate on the bract(Fig. 21); the pollinationdrop, to the epimatium(Fig. 30). The pollination therefore,adheres to theadaxial surface of the dropis secretedonto the surface of the recep- bractbase (Fig. 12).Under artificial conditions, tacle,its spreadpossibly being facilitated by dropsmay persist for several days. thepapillae (Fig. 14). Contrastbetween white, waxy,nonwettable and green, nonwaxy, wetta- Lagarostroboscolensoi -Cones areterminal ble surfacesis pronounced. on thevegetative shoots (Fig. 5) withthe ovule distalon the shortbract (Fig. 22). The drop Prumnopitysandina and P. taxifolia-The originatesfrom the micropyle(Fig. 17) and coneshave an elongatedaxis (up to 3 cm long), extendsover the adaxial surfaceof the bract withnumerous (up to 12) widelyseparated ontothe cone axis,accumulating in thebract ovules,each subtendedby one of thespirally axil;drops from adjacent ovules may fuse (Fig. arrangedbracts (Fig. 6). The mouthof the mi- 20). Furtherspread is preventedprimarily by cropyleis applieddirectly to a shallow,wetta- nonwettablewaxy deposits. blegroove, which represents the decurrent base of the bractinsertion and contrastswith the Halocarpus kirkii-This resemblesLaga- waxy,nonwettable remaining surfaces (Fig. 19). rostroboscolensoi but with the cone condensed The marginof thegroove is slightlyraised so and morerobust (Fig. 26). The fertilebracts thata veritable"gutter" is formed(Fig. 28). are less divergentso thatthe drop has a nar- Pollen is readilyobserved within the gutter, rowermeniscus and extendsfarther down the bothprior and subsequentto thesecretion of cone axis (Fig. 13). the drop.The accumulationof excesspollen in the micropylarregion of the grooveafter Lepidothamnusspp. -In Lepidothamnus dropabsorption suggests that pollen scaveng- laxifoliusthe cones are terminal on leafyshoots, ingis effective. thecone axis is condensed,and limitedreori- entationis primarilythe result of generalized Prumnopitysferruginea -Cones are borne growthcurvature of thefertile shoot. A series laterallytoward the base of previousyear oftwo or three penultimate sterile bracts forms shoots.They continue growth throughout win- a palisadethat creates a shallowopen recep- terso thata longaxis witha seriesof sterile tacle into whichthe drop extendsand is re- overlappingfleshy bracts is produced.At the tainedby capillarity (Fig. 16).A diagnosticfea- timeof pollinationthe distal part of theaxis, ture of the is the hooked micropyle whichbears a seriesof more delicate spreading (persistentin theseed) and theobliquely erect sterilebracts, elongates and becomesoriented orientationof the ovule (cf. L. intermedius,Fig. vertically.The ultimatetwo or fourbracts are 27). Underthese circumstances captured pol- narrow,cylindrical, white, waxy, and non- len travelsinitially upward into the down- wettable(Fig. 18). Usuallyonly the ultimate wardlydirected micropylar orifice. It is then or penultimatebract, in a pseudoterminalpo- drawninto the pollen chamber in thereverse sition,is fertile(Fig. 29). The bractremains directionby capillarity as thedrop either dries freeof the epimatium. The pollinationdrop is or is resorbed.The U-shapedpassage can be secretedonto the somewhat inflated cone axis reversedand repeated by reorientating the cone. and can spread extensivelyover the whole Here,then, there is an outerpollen receptacle, wettablesurface (Fig. 18). as well as a pollenchamber. Lepidothamnus intermediusis distinctin thatthe pollination OtherPodocarpaceae-Other taxa with a receptacleis morecompletely sealed because constructionthat conforms to thegeneralized thehooked micropyle seems consistently to be arrangementsuitable for pollen scavenging in- lodgedunder the tip of the opposingsterile clude ,Decussocarpus, Falcatifoli- bract(Figs. 15, 27). um,and Parasitaxus.We have observedthe lastthree close to,but not at, thetime of pol- Dacrycarpusdacrydioides-There are two or linationand havenot yet recorded pollination threebracts, fused basally to forma fleshypa- dropson them.However, the close similarity pillatereceptacle (Fig. 14). The receptacleen- in ovule orientationsuggests the same mech- largesand colorsabruptly at thetime of seed anism.These and othertaxa may be discussed dispersal.The distalpart of the bractis rep- individually(Figs. 32-37). resentedby a small waxy protuberance,de- velopedvery early in cone differentiation,the Lagarostrobosfranklini -Cones are termi- receptacleitself appearing later in association nal on vegetativeshoots, but pendulous at the withovule initiation. One (lesscommonly two) timeof pollination (A. Shapcott,personal com- September 19911 TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1299 munication).Unlike L. colensoi,the ovule is enclosingstructure, the developingseeds are morphologicallyerect and witha less well-de- indeedprotected in various ways. Brown's point velopedepimatium that encircles only the base emphasizedthat in gymnospermsonly at the of the ovule (Fig. 32). Under thesecircum- timeof pollination does pollenhave directac- stancesthe ovule is topographicallyinverted cess to theovules. Angiosperms or "enclosed and the pollen-scavengingmechanism seems seededplants," in contrast,have theirovules possible. consistentlyenclosed in a carpel,a structure preventingdirect access of pollen to the ovules, Parasitaxusustus-Cones are terminalon but witha stigmaticsurface for pollen recep- erectvegetative branches and includea single tion.Relative efficiency ofpollination in gym- pseudoterminalovule in the axil ofthe ultimate nospermsand angiospermsmust be under- or penultimatebract (Fig. 33). The micropylar stoodin theseterms. orificeis appliedto thecone axis,suitable for Pollentransfer in conifersis by windbut is pollenscavenging. evidentlyinefficient because it requireslarge amountsof pollento be dispersedrandomly Dacrydiumspp. -This genusremains prob- to a verysmall target. Increasing the efficiency lematic.In D. cupressinumthe cones are ter- ofpollen capture may be consideredselectively minalon upturnedvegetative shoots (Fig. 3). advantageous,but has beenlittle examined in The usuallysolitary ovule is inverted(Fig. 34), gymnospermsas a biologicalmechanism. Pol- butwe have notobserved a pollinationdrop. len capturein conifersmay be facilitatedby In D. araucarioides,cones are indistinctlydif- theaerodynamics ofcone construction (Niklas, ferentiatedfrom vegetative buds since the nu- 1984), but this simplyconcentrates pollen merousoverlapping outer bracts are not di- withinthe vicinity of the target. In manygym- vergentand the cone axis does not elongate nosperms,as in mostconifers, the size of the (Fig. 35). One ortwo ovules occupy the central ultimatesite for pollen reception is increased cavitysurrounded by the palisade of sterile bythe secretion of a dropof fluid, which exudes bracts.Ovules are invertedand subtendedby fromthe micropyle and remainsfor some pe- a largebract. It is difficultto understandhow riodof time (Fig. 10).Other mechanisms occur pollenreaches these structures, which are com- and are clearlyderived within the gymno- pletelyenclosed. More field work on this widely sperms(Doyle, 1945). However,if we accept distributedgenus is required. theclaim of Rothwell(1 977) forthe existence of pollinationdrops in fossilovules of Car- Decussocarpuscomptonii -Cones arelateral boniferousgymnosperms, then the pollination on previousseason's vegetative shoots, with a dropis an ancestralfeature in moderngroups. singlesubterminal ovule (Fig. 36). Bractand Interest,therefore, centers on a mechanismthat epimatiumare free. mayincrease the efficiency of pollinationand be a majorfeature of the reproductive biology Falcatifoliumtaxoides-There is a single of Podocarpaceae.The relativelyfew podo- subterminalovule surrounding the epimatium, carps witha cone morphologynot suitedto usuallywith the tip of a sterilebract opposed the mechanism(, Phyllocladus, (Fig. 37). Againthe micropyle faces the upper Saxegothaea)may be interpretedas eitheran- partof thecone axis. cestralor derived.Saxegothaea is clearlyde- rived,because of its many structural peculiar- DISCUSSION ities;it lacks a pollinationdrop, and thepollen germinatesaway from the ovule (Noren, 1908; RobertBrown (1827) distinguishedgym- Doyle and O'Leary, 1935; Looby and Doyle, nospermsfrom angiosperms most precisely on 1939).It parallels,in thisrespect, the situation thebasis of the mechanism of pollen reception. in a numberof Pinaceae that lack a pollination He pointedout that in gymnosperms the ovule drop(Doyle, 1945;Owens and Molder,1975), receivesthe pollen directly; that is, thepollen moststrikingly in thegenus Hesperopeuce (= mustbe capturedby themicropylar orifice of Tsuga mertensiana;Page, 1989). This simi- theovule (cf. Fig. 10),but in angiospermsthe larityamong the two families is assumedto be pollenis receivedby the stigmaof the ovary a convergencebetween distinct phyletic lines. and gametesare deliveredto the ovule by a On theother hand, the -mechanism known for pollentube. The distinctionis functional,but Phyllocladus,and presumedfor Microstrobus, is usuallytranslated into structural terms since seemsancestral within the family since it cor- gymnospermsor "naked seeded plants" are respondsto the typegeneralized within the definedby their "naked" ovules. However, al- gymnosperms(and apparentlycharacterizing thoughthey lack any consistentlyspecialized the familiesCephalotaxaceae, , 1300 AMERICAN JOURNAL OF BOTANY [Vol. 78

Taxaceae,and Taxodiaceaein theirentirety). bractsand withthe morphology at thetime of An extensionin time ofthe pollen capture pro- pollinationrelated to the"pollen scavenging" cess is knownfor Picea and Pinus. Here the process.Commonly there is a relativelyspe- ovule is providedwith a pair of micropylar cialized area (Fig. 11, Zone X) adapted for armsthat secrete minute "droplets," rendering receptionof pollenand the pollinationdrop. thearms viscous. Pollen can adhereto these The aberrantgenera Phyllocladus and Micro- armsand be pickedup subsequentlywhen the strobusare placed in thistraditional scheme as normalpollen drop, secreted by thenucellus, derivedentities, the epimatium in Phyllocladus is produced.Effectively this extends the period beinghomologized with the arillatestructure of pollenreception by theovule, as discussed thatdevelops late in cone ontogeny(Tomlin- by Owens,Simpson, and Molder(1987) and son,Takaso, and Rattenbury, 1989), unlike the constitutesa minimalkind of pollen scaveng- epimatium,which is a necessaryprecursor to ing. ovuleinitiation (Tomlinson, unpublished data). If one acceptsthis comparative interpreta- The simplestcondition, that of Microstrobus tion,then the cone morphology of the majority (Fig. 31), is thenconsidered to be totallyde- of podocarpspossessing inverted ovules rep- rivedby reduction. The overallpicture invokes resentsa derivedcondition specialized in re- theevolutionary loss of the epimatium, the aril lationto a processthat renders pollination more in Phyllocladusbeing its vestige.Clearly, this efficient.This immediatelyraises the question picturedepends on an interpretationof the ofthe morphological nature of the epimatium, epimatiumsolely in conventionalterms and is whichis absentfrom Microstrobus and Phyl- supportedby vascularanalysis and compara- locladus,since there is sucha closecorrelation tivemorphology of mature cones (Stiles, 1912; betweenthe presence of an epimatiumand the Sinnott,1913; Wilde, 1944). Florin (1951, secretionof a pollinationdrop. In theconven- 1954) incorporatedthis view into his gener- tionalview generatedby Sinnott(1913) and alizedpicture of cone reduction in conifersbut acceptedby subsequentauthors (e.g., Wilde, made no newobservations. 1944; Florin,1954), part for part comparison In biologicalterms, the function of the epi- of the axillaryfertile complex of the ovulate matiumhas been little discussed. The structure cones of Pinaceae and Podocarpaceaeis pos- has no consistentrole in the developmentof sible (Fig. 38). In Pinaceae,there is a pair of the fleshinessthat characterizes the dissemi- ovules insertedbasally and withinverse ori- nulesand is essentialto their dispersal. A fleshy entationon a scale (the ovuliferousscale) in structurecan be producedin a diversityofways theaxil of each fertilebract. The ovuliferous (Fig. 38, lowerleft). For example,in Dacry- scale itselfis homologizedwith the reduced carpusa fleshyreceptacle is formedby the base branchaxis found in somepresumed ancestors of thebracts beneath the seed, the distal part (theCordaitales and extinct transitional groups of the fertilebract being adnate to the epi- of ). matium,which is not fleshy.Podocarpus is Thispaleobotanical evidence was assembled somewhatsimilar, but the bract is notadnate. bythe extensive comparative studies of Florin In Dacrydiumthe epimatiumenvelopes only (e.g., 1951, 1954). The singleovule of podo- thebase ofthe seed, which is otherwiseexposed carpshas, for the most part, the same inverted (Fig. 34). In Prumnopitysthe epimatiumbe- orientationas in Pinaceae,and thepresumed comesthe attractive fleshy structure, the bract ovuliferousscale is conventionallyhomolo- remainingunelaborated (Fig. 38). In taxa like gizedwith the epimatium, which often encloses Lepidothamnus,the epimatium, which is rel- the ovule to greateror lesserextent. Support ativelyconspicuous at thetime of pollination, forthe homology of epimatium with the ovu- showslittle further enlargement in thematu- liferousscale comes fromcomparative anat- rationof the seed (Fig. 27), thebasal portion omy.Both structureshave a vascularsupply of the cone axis becomesred and fleshy,the in whichxylem and phloemhave an inverted seed coat becominga contrastedblack. These orientation(Fig. 38), i.e., withxylem abaxial fewexamples illustrate the divergentdevel- ratherthan adaxial (Sinnott,1913). The sim- opmentalpossibilities during seed maturation, plest(but not necessarilyancestral) condition involvingvarious parts of thesehighly spe- is thenrepresented by taxa likeMicrocachrys cialized cones and withoutconsistent partici- and Saxegothaea,with a moreobvious cone- pationof theepimatium. likeorganization, since each cone has several An alternativeto theidea thatevolution in fertilebracts. Saxegothaea is, however,spe- cone morphologyof podocarps has proceeded cializedin itspollination mechanism. In most by specializationand ultimatelyloss of the otherpodocarps, the seed cones are highly spe- ovuliferouscone can be based on the polli- cialized,commonly with only one or two fertile nationmechanism. In thisinterpretation, the September19911 TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1301

() PINACEAE lPODOCARPACEAE

ovule epimatium

bract ~~~~~~~~~~bract m rn j 1 - phloem . MICROCACHRYS _ SAXEGOTHAEA 2r -I 0 F (n ic Cn ep_m mepimatium

atum eOOA pimoatiumi MOST bract PODOCARPS fDISSEMINULE

lW zS \\ ' ~~~~~~~~receptacle||l

RUMNOPITYS ZONE X X recepta ovule no receptacle

aril I: ~~~~ovule LEPIDOTHAMUS

9 receptacle

PHYLLOCLADUS MICROSTROBUS Fig. 38. Evolutionarymorphology of the podocarpaceous cone. Pinaceae: the conventional interpretationof the ovuliferousscale as a branch homologue with invertedvascular bundles. Podocarpaceae: the same configurationwith the ovuliferousscale an epimatium,as in Microcachrysand Saxegothaea. The arrangementin most podocarps with one to two ovules per cone and the pollinationmechanism described here may be derived fromthe conditionin these two genera.Phyllocladus and Microstrobosthen represent the ultimatereduction, with the epimatiumreduced to a late- developingaril (Phyllocladus);or whollyabsent (Microstrobus).This implies loss of the epimatiumas an evolutionary trend(arrow, right). In the developmentof the seed (S) into a fleshydispersal unit in 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 pollination mechanism is considered,as we hypothesize. epimatiumhas arisen de novoand it represents transitionconifers, e.g., Ullmannia(Stewart, a structureintimately associated with the pol- 1983). Preliminarydevelopmental evidence len scavengingprocess. An ancestryfor the shows that the epimatiumalways precedes Podocarpaceaewithin a groupthat may have ovuleinitiation in sucha waythat it produces lackedan ovuliferousscale may not be difficultthe inverted ovule orientation, an essentialin- to postulate,since the condition occurs in the gredientof the pollen scavenging mechanism. 1302 AMERICAN JOURNAL OF BOTANY [Vol. 78

One mustemphasize that ovules in gymno- cialized mechanismsin theirpollination bi- spermsare alwaysorthotropous and have no ologyshows that their further detailed exam- inherentmechanism for reorientation (unlike inationcan be pursuedwith scientific benefit, angiospermswith their frequent double integ- especiallyas increasingemphasis has beenput umentsand inherentcapability for curvature). on pollinationas theadaptive driving force for Epimatiumand outerintegument may have theorigin and specializationof the seed habit equivalentbiological properties, but this is not (Haigand Westoby,1989). However, one can- to implythat they are homologues.The con- notdisassociate one aspectof the reproductive ventionalevolutionary scenario presented in processfrom another. A characteristicfeature Fig.38 thuscan be reversed,with Microstrobus of most podocarps is a disseminulecomposed and Phyllocladusbeing the antecedenttypes, of a largeseed and associatedfleshy, brightly reflectedin theirerect ovules and simplepol- coloredstructures and correlatedwith animal linationmechanism. The aril of Phyllocladus dispersal.Selection for this dispersal unit seems couldthen be theprecursor for the epimatium directedtoward reduction of ovule number per thathas becomethe characteristicfeature of cone. A typologicalreduction series exists mostpodocarps, but as a derivedand not an withinthe family; this may mirror the inter- ancestralstructure. Lagarostrobos franklinii dependencebetween pollination efficiency, seed couldfit into this picture since ovule inversion biology,and cone morphology.Podocarps is determinedby cone inversion(Fig. 32). clearlyhave distinctivedemographic proper- Otheraspects of the structure and biology of ties(Ogden, 1985) as wellas unusualseed and podocarpscomplicate both evolutionary sce- seedling strategies(Philipson and Molloy, narios.Pollen in mostpodocarps is saccate,or 1990),all ultimatelydependent on highlyde- winged(Tegner, 1965; Pocknall,1981), i.e., rivedcone morphologies. Continued field work withtwo or threebladderlike extensions of the on the familyshould be pursued,because it exine(as in thefamiliar textbook illustrations will clarifythe systematicsand relationships of Pinus). Doyle (1945) suggestedthat these ofthisdistinctive and important southern group structureswere essential for maintaining pollen of plants. buoyancyin thepollen drop, but not in air.He noteda closecorrelation between the presence LITERATURE CITED ofwinged pollen and a pollinationdrop in Pi- naceae. A similarsituation may existin Po- BROWN,R. 1827. Characterand descriptionof Kingia; docarpaceae;Saxegothaea lacks wingedpol- a new genus of plants found on the south-westcoast of New Holland. With observationson the structure len.In Phyllocladusthe wings can be described ofits unimpregnated ovulum, and on thefemale flower onlyas vestigial.Dacrydium lacks wingsfor of Cycadeae and Coniferae.Reprinted from narrative themost part, according to Tegner(1965), but of a survey of the intertropicaland Western Coasts not D. cupressinum,according to Pocknall of performedbetween the years 1818 and (1981). Clearlythe situationdeserves reex- 1822, Captain Philip P. King R.N., F.R.S., F.L.S., vol. aminationin thefamily as a whole.A further 2. London. DE LAUBENFEIS, D. J. 1972. Flore de la Nouvelle Ca- biological mechanismproposed by Doyle l6donie et Dependances vol. 4. Gymnospermes.Mu- (1945) was thatpollen wings guaranteed a pre- seum National d'histoirenaturelle, Paris. ferredorientation of the pollen on thenucellus 1988. Coniferalesin Flora Malesiana, series 1, in orderto facilitatepollen germination. Ob- vol. 10 (3). Martinus Nijhoff.The Hague. servationsby Lill and Sweet(1977) on Pinus DOYLE, J. 1945. Developmental lines in pollinating radiatado not supportthis idea. mechanismsin the Coniferales.Scientific Proceedings of theRoyal Dublin SocietySeries A 24: 43-62 (New Dacrydiummay be a keygenus in thesebi- series). ological interpretations.It apparentlylacks , AN M. O'LEARY. 1935. Pollination in Saxe- pollenwings, has a cone morphology,seem- gothaea. ScientificProceedings of the Royal Dublin inglywith totally enclosed ovules, and no pol- Society 21: 175-179. linationdrop has yetbeen reported.The pre- EAMES, A. J. 1913. The morphologyof australis. observationsshould be Annals of Botany (London) 27: 1-38. liminarynature of our FLowN, R. 1951. Evolution in and conifers. clearfrom this discussion, but points the way Acta Horti Bergiana 15: 285-388. to fiurthernecessary field work and directob- 1954. The femalereproductive organs of conifers servationof themechanism. and taxads. Biological Reviews 29: 367-389. The Podocarpaceae, with an intriguing HAIG, D., AND M. WESTOBY. 1989. Selective forces in ""distribution, have been relative- the emergenceof the seed habit. Biological Journalof the Linnean Society of London 38: 215-238. lyneglected by botanists, and the role they play HAmmNS,R. J., N. PRAKASH, AND D. J. NIKLEs. 1984. in interpretingevolutionary processes in co- Pollination in Araucaria Juss. Australian Journal of nifershas been minimized,largely because of Botany 32: 583-594. ignorance.The currentdemonstration of spe- LILL, B. S., ANDG. B. SWEET. 1977. Pollinationin Pinus September19911 TOMLINSON ET AL. -POLLINATION IN PODOCARPACEAE 1303

radiata.New Zealand Journalof Forest Research 7: Prumnopitys.New Zealand Journalof Botany 28: 73- 21-34. 84. LOOBY, W. J.,AND J. DOYLE. 1939. The ovule,game- POCKNALL,D. T. 1981. Pollenmorphology of the New tophytesand proembryoin Saxegothaea.Scientific Zealand species of Dacrydium Solander, Podocarpus Proceedingsof the Royal Dublin Society 22: 95-117. L'Heritier,and DacrycarpusEndlicher (Podocarpa- NIKLAS,K. 1984. Themotion of windborne pollen grains ceae). New Zealand Journalof Botany 19: 67-75. aroundconifer ovulate cones: implications on wind QuINN,C. J. 1970. Genericboundaries in thePodocar- pollination.American Journal ofBotany 71:356-374. paceae. Proceedings of the Linnean Society of New NOREN,C. 0. 1908. ZurKenntnis der Entwicklung von South Wales 94: 166-172. Saxegothaeaconspicua Lindl. Svensk botaniska Tid- * 1982. Taxonomyof DacrydiumSol. ex Lamb. skrift2: 101-122. emendde Laub. (Podocarpaceae).Australian Journal of Botany 30: 311-320. OGDEN, J. 1985. An introductionto demography * 1987. The Phyllocladaceae-acritique. Taxon withspecial reference to NewZealand trees. New Zea- 36: 559-565. landJournal ofBotany 23: 751-772. ROTHWELL,G. W. 1977. Evidencefor a pollination-drop OWENS,J. N., ANDM. MOLDER. 1975. Sexualreproduc- mechanismin Paleozoicpteridosperms. Science 198: tionin mountainhemlock (Tsuga mertensiana).Ca- 1251-1252. nadianJournal of Botany 53: 1811-1826. SINNoTT,E. W. 1913. The morphologyof the reproduc- , S. J. SIMPSON,AND G. E. CARON. 1987. The tivestructures inthe Podocarpaceae. Annals ofBotany pollinationmechanism of Engelmannspruce (Picea (London) 27: 39-82. engelmannii).Canadian Journal ofBotany 65: 1439- STEWART, W. N. 1983. Paleobotanyand theevolution 1450. ofplants. Cambridge University Press, Cambridge. , AND M. MOLDER. 1981. Sexualrepro- STILES,W. 1912. The Podocarpeae.Annals of Botany ductionof Pinus contorta. I. Pollendevelopment, the (London) 26: 443-514. pollinationmechanism and early ovule development. TAKAso,T. 1990. "Pollinationdrop" time at theArnold CanadianJournal of Botany 59: 1828-1843. - Arboretum.Arnoldia 50: 2-7. PAGE, C. N. 1989. New and maintainedgenera in the TEGNER, J. 1965. Dacrydium-anatomyand . coniferfamilies Podocarpaceae and Botaniska Notiser 118: 450-452. Pinaceae.Notes * fromthe Royal Botanic Gardens, Edinburgh 45: 377- 1967. Anatomyand taxonomyin thePodocar- 395. paceae. Botaniska Notiser 120: 504-506. TOMLINSON,P. B., T. TAKASO,AND J. A. RATTENBURY. 1990. Coniferophytina(Conifers and Gink- 1989. Coneand ovuleontogeny in Phyllocladus (Po- goids).In K. Kubitzki[ed.], The familiesand genera docarpaceae). Botanical Journal of the Linnean So- ofvascular plants, vol. 1, SpringerVerlag, Berlin. ciety99: 209-221. PHILiPSON,W. R., AND B. P. J. MOLLOY. 1990. Seedling, WILDE,M. H. 1944. A newinterpretation ofconiferous shoot,and adult morphology ofNew Zealand conifers. cones. I. Podocarpaceae. Annals of Botany (London) Thegenera Dacrycarpus, Podocarpus, Dacrydium and 8: 1-41 (New series).