On the occurrence of non-axillary ovules in Tetraclinis ... the occurrenc… · On the occurrence...

Feddes Repertorium 114 (2003) 7–8 , 497–507 DOI: 10.1002/fedr.200311012 Weinheim, Dezember 2003

© 2003 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 0014-8962/03/7-812-0497

Ruhr-Universität Bochum, Spezielle Botanik, Bochum

A. JAGEL & TH. STÜTZEL

On the occurrence of non-axillary ovules in Tetraclinis articulata(VAHL) MAST. (Cupressaceae s.str.)1

With 7 Figures

1 Dedicated to Professor Dr. Dietrich Müller-Doblies, Berlin on the occasion of his 65th birthday.

Summary

The cone morphology in Tetraclinis was studied toelucidate the taxonomic position of the genus. Acareful analysis of the cone development shows thatthe characters used as arguments for an affiliationwithin Callitroideae are superficial and of littletaxonomic significance. The developmental patternsindicate a position of Tetraclinis within Cupressoi-deae. Tetraclinis displays ovules inserted directly atthe distal end of the cone axis and not born in theaxil of a seed scale as recently shown for Juniperus(SCHULZ et al. 2003) and Microbiota (JAGEL &STÜTZEL 2001b). The close relationship betweenTetraclinis, Juniperus and Cupressus as suggestedby SAXTON (1913) based on embryological data, byGADEK & QUINN (1985) based on biflavones and byGADEK et al. (2000) based on DNS-sequences issupported by the morphological data presented here.Conflicting morphological concepts or morphologi-cal trees (e.g. GADEK et al. 2000) are in parts weaklysupported and suffer either from ambiguous codingof morphological data or are based on historicalmorphological errors. To calculate reliable mor-phological trees, however, requires data of similarquality and cannot be achieved by using data whichare tailed to the use in effective diagnostic keys.

Zusammenfassung

Zum Vorkommen von nicht-axillären Samen-anlagen bei Tetraclinis

Die Zapfenmorphologie von Tetraclinis wurde un-tersucht, um die systematische Stellung der Gattungzu erhellen. Die sorgfältige Analyse der Zapfenent-wicklung zeigt, dass die Argumente, die bisher füreinen Einschluss in die Callitroideae herangezogenwurden, das Ergebnis von oberflächlicher Betrach-tung oder aus anderen Gründen wenig aussagekräf-tig sind. Die Entwicklungsmuster legen eine Stel-lung in den Cupressoideae nahe. Tetraclinis zeigtam distalen Zapfenende Samenanlagen, die direktan der Zapfenachse und nicht in der Achsel einerZapfenschuppe (Deckschuppe) inserieren, wie dieszuvor für Juniperus (SCHULZ et al. 2003) und Mi-crobiota (JAGEL & STÜTZEL 2001b) gezeigt wurde.Die enge verwandtschaftliche Beziehung zwischenTetraclinis, Juniperus, und Cupressus, wie sie be-reits von SAXTON (1913) auf der Basis von em-bryologischen Daten und von GADEK & QUINN(1985) auf der Basis von Biflavonen sowie vonGADEK et al. (2000) auf der Basis genetischer Ana-lysen postuliert wurde, wird von den hier vorgeleg-ten morphologischen Daten gestützt. Konträre mor-phologische Ansichten oder Stammbaumrekonstruk-tionen auf der Basis morphologischer Daten (z. B.GADEK et al. 2000) sind in wichtigen Punkten nurschlecht gestützt, das Ergebnis von zweideutigenoder sogar falschen Kodierungen der Merkmale, diez. T. auf sehr alten historischen Irrtümern basieren.Für die Berechnung verlässlicher morphologischerStammbäume sind vergleichbar zuverlässige Datenfür weitere Gruppen erforderlich. Dies kann nichterreicht werden, indem Daten, die für die Verwen-dung in Bestimmungsschlüsseln erhoben wurden, inphylogenetischem Kontext zweitverwendet werden.

498 Feddes Repert., Weinheim 114 (2003) 7–8

© 2003 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Introduction

The monotypic genus Tetraclinis is mainlydistributed in the Atlas Mountains in northwestAfrica. Apart of this main area, some smallrelict areas exist in Tunisia, the Cyrenaica,Malta and in southeast Spain (TEMPLADO1975). A fertile fossil record of the MiddleMiocene was discovered in Croatia by KOVAR-EDER & KVA�EK (1995). In the “preliminaryworld list of threatened conifer taxa” byFARJON et al. (1993) it is rated as vulnerable. InCentral Europe Tetraclinis articulata is nothardy (KRÜSSMANN 1983) and mostly culti-vated in the temperate house. Thus, the speciesis rarely to be found in Botanical Gardens.

Within Cupressaceae s.str., the monotypicgenus Tetraclinis MAST. was included in theCallitroideae by LI (1953), a classificationwhich was prevalent for a long time (e.g.KRÜSSMANN 1983). In this subfamily, Tetra-clinis is exceptional because all other membersare distributed exclusively in the southernhemisphere while Tetraclinis occurs in themediterranean region. As only argument forthis affiliation LI (1953) emphasizes the val-vate cone scales of the ripe cones which seemto be similar to the condition in all remainingmembers of the Callitroideae. In the past fewyears, the systematic position of Tetracliniswas questioned and newly discussed. In treesbased on different molecular analyses, Tetra-clinis came out together with the northernhemispherical Cupressoideae (BRUNSFELDet al. 1994; GADEK et al. 2000). SAXTON(1913) placed Tetraclinis also in his Cupres-soideae, based on embryological studies, aposition within Cupressoideae is also supportedby biochemical studies (GADEK & QUINN1985). The resulting conflict between the mor-phological approach on the one hand and themolecular and embryological approach on theother hand was widely ignored up to now.While a position of Tetraclinis within Cupres-soideae seems well supported by most of themore recent studies, the affiliation of Tetra-clinis within Cupressoideae remained stilldoubtful.

A survey on the bibliography, however,reveals that the morphological data for Tetra-clinis itself are far from being consistent andcomplete. The cone morphology of Tetraclinis

is in fact very similar to that of e.g Widdring-tonia in respect to the very short cone axis andthe only four (fertile) valvate cone scales. Butthese characters are weak in indicating basi-cally reduced cones and allowing no cleardistinction between Callitroideae and Cupres-soideae. Other available data are confusing andoften contradictory. This applies especially tothe number and position of the ovules within acone. At a first glance it seems that the (usu-ally) six seeds per cone are born in two groupsof three in the axils of the proximal pair ofscales, whereas the distal two cone scales aresterile. This impression is underlined by thearrangement of the very wide seed wings(Fig. 1D, Fig. 2). Amongst others, this inter-pretation was given by KRÜSSMANN (1983)who described the lower seed scales as fertile,bearing two or three seeds each. On the otherhand, PABST (1887) assigned one seed to eachof the upper two seed scales and two or three tothe lower ones. A very doubtful number percone scale is published by HORA (1981), whoindicated two to nine (!) seeds per seed scalewithout a more precise allocation to conescales. This would result in a total number ofseeds per cone which has never been found byany author and not by us either. Most of thepublications do not specify the location of theseeds at all, e.g. PILGER 1926, DALLIMORE &JACKSON 1966, PAGE 1990.

To clarify these systematic and morpho-logical problems, we examined mature andyoung cones of Tetraclinis articulata andstudied the morphogenesis. The results arecompared with those for other Cupressaceae(JAGEL & STÜTZEL 2001a, b; JAGEL 2002;SCHULZ et al. 2003).

Material and methods

Early developing and ripe cones were collected fromcultivated plants at the Botanical Gardens ofDüsseldorf and Bonn (North Rhein-Westphalia,Germany). The material was fixed in FAA for atleast half a day and then transferred and preserved in70% alcohol. Young cones were dissected and mostof the cone scales removed. For SEM studies theywere then dehydrated in FDA and critical pointdried and coated with gold-palladium using aBalzers sputter coater. Different cone types weredepicted as cone diagrams using CorelDraw 9.0.

A. JAGEL & TH. STÜTZEL: Occurrence of non-axillary ovules in Tetraclinis articulata 499


Results

The ovulate cones of Tetraclinis are formedterminally on short shoots. Just at the begin-ning of the cone formation, the reproductiveshoots are bent down into a horizontal (plagio-tropic) position. Thus, the pollination dropletsare exposed in this direction as well. The lasttwo pairs of leaves below the cone are transi-tional between vegetative leaves and conescales being much shorter than normal vegeta-tive leaves. The cone itself consists always oftwo pairs of scales. At pollination, the conescales are already swollen at the base. The tipsof the cone scales are thus spreading and givethe flowering cone a star-like appearance in topview. This is unusual within the Cupressoi-deae, and apart from Tetraclinis only found inJuniperus sect. Sabina. At the distal end of thecone, no terminal piece (“columella”, see alsoJAGEL & STÜTZEL 2001a) is developed, andnormally no trace of the end of the cone axiscan be found. But sometimes a rudimentaryand undifferentiated apex could be found inyounger developmental stages hidden betweenthe inner ovules (Fig. 3). The shape of thisrudiment resembles the situation in the conesof Widdringtonia schwarzii (see JAGEL 2002).The seed scales as well as the scale leaves aredecussate, although in some publications theyare described as arranged in whorls of four(e.g. DALLIMORE & JACKSON 1966; KRÜSS-MANN 1983; PAGE 1990; GADEK et al. 2000).The decussate arrangement is proved by devel-opmental studies of the cone apex and can bedetected even from mature stages under a dis-secting microscope. The strange habit resultsfrom a regular alternation of a long and a veryshort internode.

Pollination in both individuals studied oc-curred at a quite different time. The plant in theBotanical Garden of Bonn developed pollina-tion droplets at the beginning of November in1999 in the temperate house. The youngestdevelopmental stages of these cones had beenfound in July of the same year. Thus, the coneshad passed a resting period of some months asit is the usual case within the Cupressaceae. Onthe other hand the plant in the Botanical Gar-den of Düsseldorf flowered already at the be-ginning of August in 2001, at a time, when ithad been removed from the greenhouse to the

open air. Unfortunately, the earliest develop-mental stages of these cones have not beenobserved by us, but they have obviously notpassed such a long resting period. Although thecultivating conditions of both plants are quitesimilar, the differences in pollination timeshould be best regarded as a cultivation arte-fact. In its natural range in Spain the pollina-tion of Tetraclinis articulata takes place be-tween September and November (TEMPLADO1975).

Twigs with flowering cones were collectedin the Botanical Garden of Bonn and trans-ported to the Ruhr-University in Bochum.Being put into a vase, the ovules developedpollination droplets again. At first each ovuleformed a single pollination drop (Fig. 1A). Inlater stages the pollination droplets increasedand finally fused with the droplets of theneighbouring ovules (Fig. 1B, C). Such a fu-sion of pollination droplets has been observedin other genera of Cupressaceae, e.g. in Cu-pressus (JAGEL & STÜTZEL 2001a) and Junipe-rus sect. Sabina (SCHULZ et al. 2003), Fitzroya,and some others (JAGEL 2002). This feature isso far known only from within Cupressaceaes. l . and probably represents an advantage incatching the pollen grains, due to the muchlarger diameter of the droplets which allows amore effective exposition of the droplet. Thefusion is not a pruning artefact and can beobserved in situ in the Botanical Garden, too.

Most of the cones of Tetraclinis articu-lata develop a total number of six ovules(Fig. 4A 1). The development of such cones isshown in Fig. 5A–C. The innermost ovules ofthe cone develop first (marked with “1”), fol-lowed by two ovules at each side of the cone(marked with “2”). These four ovules developmore or less simultaneously, and they are sig-nificantly younger than the first two ones. Insome cases more than six ovules are formed,and an additional ovule appears between onepair (Fig. 4B 1) or between each pair (Fig. 4C1)of the younger ovules. The developmental leadof the first two ovules is maintained until polli-nation (Fig. 1A, B). In very rare cases, one canfind cones with eight ovules in a different ar-rangement. Compared to the most frequenttype with six ovules, two additional ovulesdevelop in median position to the uppermostscales (Fig. 1F, arrows). The scars remaining



Fig. 1Tetraclinis articulata

A — Cone at the beginning of pollination. The droplets areseparated from each other; B, C — Cone at pollinationtime with fused, much larger pollination drops; D —Young cone after pollination time. The seed wings areorientated in the same direction; E — Mature cones; F —Rarely found type of mature cone with seed scars in theaxils of the uppermost pair of cone scales

after seed shed of the two most distal ovulesare at right angle to the scars of the other ones.As cones with more than six ovules have beenrare in both examined plants (and seem to berare in the species at all) we could not findearly developmental stages of such cones.

The mature cones of Tetraclinis articulata(Fig. 1E) are best described as having a cube-like shape in the closed state and are orientatedmore or less erect. The inner cone scales areslightly narrower than the outer ones. The outersurface of the cone scales is prominently con-cave, and the original leaf tip forms a back-ward-curved hook in the distal third of thescale. The seeds have very broad wings whichare broader than the seed itself (Fig. 2). Therelative position of the wings in a transversalsection is shown for all seeds in the cone inFig. 4, second column. Due to the saddle,

shaped insertion of the fertile cone scales, thewings are elongated proximally (Fig. 6B).After seed shed, a narrow ellipsoidal scar re-mains on the cone axis, which can easily beseen in older cones due to its dark colour(Fig. 1F). The orientation of these scars withinthe different cone types is shown in Fig. 4,third column.

Discussion

The contradictory information in literatureabout the position of the ovules or seeds seemsto be based on interpretations of the orientationof the seed wings in the ripe cone. These ob-servations do not consider the morphogenesisof the cone nor the seed scars in the ripe conesalthough these features are obviously essentialfor the understanding of the seed cone in Tetra-clinis articulata.

Looking at the most frequent cone typewith six ovules, one might assume that they aregrouped by three in the axils of the last but onewhorl of cone scales. A position of any ovuleor combination of ovules in the axils of theuppermost whorl would lead to a constantasymmetric arrangement what is in full con-trast to the highly symmetric architecture of thecone. But if interpreted as groups of three, this


Mature seeds. A — Seed of an uppermost ovule with the scar showing same orientation as the wings; B — Seed born inthe axil of a last but one cone scale with the scar orientation in a right angle to the wings. The arrows indicate the abscis-sion scars

�




Rudimentary and undifferentiated apex (arrow) in a young-er developmental stage hidden between the two most distalovules (OV) (removed)

would imply at the same time a centrifugalinitiation sequence for the ovules within a row.This would be in contrast to the centripetalinitiation sequence which has been proved forall Cupressaceae hitherto investigated (JAGEL2002). In genera with a seemingly centrifugalformation (Chamaecyparis), it could be shownthat the pattern is centripetal, e.g. derived froma basipetal sequence of several rows of ovulesfollowing a centripetal pattern within the row(JAGEL & STÜTZEL 2001a). Furthermore, wecould not yet find any species in which thedifference in size between the ovules of a sin-gle row was as prominent in early stages as inTetraclinis (Fig. 5A).

Sometimes the ovules are grouped to four.In this case (Figs. 5D–F) the fourth ovule is inmedian position basal to the first ovule to de-velop. This might be interpreted as two rows ofovules in the axil of one scale with either thefirst row consisting of three ovules and thesecond one with a single one or vice versa. Asthe first (most distal) row is generally bestdeveloped and displays the largest number ofovules, one can hardly assume, that the firstrow comprises only a single ovule. In case thefirst (distal) row is regarded as being composed

of three ovules, the initiation sequence iswrong in comparison to the other genera of thefamily.

The scar that is left after seed shed givesadditional and convincing evidence, that theovules in groups of three or four are not axil-lary to the same cone scale. Looking at thescars left after seed shed, e.g. in Cupressussempervirens (Fig. 6A, Fig. 7), one can seethat all the scars of a single row are paralleland at right angle to the insertion zone of thesubtending scale. Subsequent rows exhibitexactly the same orientation. In Tetraclinis,however, the scar of the larger distal ovule is atright angle to the other ones (Fig. 4A 3, 4B3,4C3). This ovule can hardly be axillary to thesame scale as the more basal ovules. Thesometimes formed fourth ovule, however, hasits scar parallel to the lateral ones and is there-fore part of a group of three in the axil of thelast but one whorl of cone scales. As a singleovule in the axil of a cone scale is always posi-tioned in median position to the scale (SCHULZet al. 2003), the distal pair of ovules cannot beregarded as axillary product of the distal conescales and cannot be confined to any of thecone scales.

We therefore are convinced that the mostdistal two ovules are not axillary to any of thecone scales, but are parts of a seed scale (ovulebearing brachyblast) terminating the cone axis(see SCHULZ et al. 2003). The two ovules takethe position and display the shape of the inser-tion zone, which is expected for a third whorlof leaves. This interpretation explains also whythey are ahead in development in comparisonto the other ones. The meristem in the axils ofthe cone scales must first be formed, the mer-istem of the cone axis is still present. The ovu-lar scars are always transversal to the axis towhich the ovule belongs. The axillary ovulesare part of an axillary short shoot (seed scale)and have there scars at right angle to the leafbase of the cone scales. The ovules of the ter-minal short shoot for the same reason havetheir scars parallel to the leaf base of the pre-ceding cone scales (Fig. 6B). The decussatearrangement of the cone scales is probably thereason why this pattern has not been recog-nized earlier. In cones with spiral arrangementof the cone scales, the ovules of the terminalshort shoot would never be placed in perfectly



A1

B1

C1

D1 D2 D3

C2 C3

B2 B3

A2 A3


A – D — Diagrams of different cone types. First column (1): at pollination time, second column (2): at ripeness; thirdcolumn (3): ripe cones after seed shed showing the orientation of the seed abscission scars. A — most frequently foundtype with six ovules/seeds, B — Type with three ovules/seeds on one of the last but one cone scales,C — Type with three ovules/seeds on the last but one seed scales each, D — Type with fertile uppermost seed scalesColours of the scales: white: normal scale leaves; light grey: transitional leaves; dark grey: cone scales; black: backward-curved hook on the backside of the scone scales indicating the tip of the scale primordium

median position to a lower cone scale as it isthe case in Tetraclinis, and therefore could notbe mixed up with those being axillary to ascale. As the seed wings are formed very late,

their orientation does not reflect the develop-mental pattern. They obviously fill the avail-able space and this leads to an orientationwhich obscures the bauplan.

A1 A2 A3

B1 B2 B3

C1 C2 C3

D1 D2 D3



Fig. 5Tetraclinis articulataCone development. A– C — Development of the mostfrequently found cone type with six ovules per cone. Theinnermost ovules of the cone develop first (in A markedwith “1”), followed by two ovules at each side of the cone(in A marked with “2”). D– F — Cone with three ovules inthe axils of both last but one cone scales, the median oneon the right side is aborted in an early stage of develop-ment as can be seen from Fig. F (arrow). A – D — topview, E, F — lateral viewFCS = fertile cone scale, SCS = sterile cone scale

With ovules inserted directly at the coneaxis and not axillary to any cone scale, Tetra-clinis displays the same phenomenon as Juni-perus sect. Juniperus (SCHULZ et al. 2003) orsome cone types in Microbiota (JAGEL &STÜTZEL 2001b). The morphology of thecones therefore fits perfectly for Cupressoideaeand such a phenomenon could not be foundwithin the Callitroideae. A closer affinity between Tetraclinis and Chamaecyparis is pro-

Fig. 6Scheme of development and orientation of seed scars in Cupressus sempervirens (A) and Tetraclinis articu-lata (B)

In Cupressus the scars remain after seed shed are elongated at right angle to the insertion zone of the fertile cone scale inall rows of ovules. If a row of ovules is regarded as a lateral axis bearing ovules instead of leaves, the insertion zone isenlarged always transversal to the axes the organs are inserted on. If the bauplan of Cupressus applies to Tetraclinis, theuppermost two ovules cannot be axillar to whorl 1 because of the wrong orientation of the abscission scar. The scar has inthis case the orientation which would be expected for a third whorl of leaves. It is therefore suggested that these ovulestake the position of an additional whorl of leaves and are inserted directly at the cone axis. This interpretation goes in linewith other important developmental characters

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Fig. 7Cupressus sempervirens

Adaxial side of a mature seed scale after seed shed.The scars are orientated in a right angle to theinsertion zone of the subtending scale



posed by ALVIN et al. (1982) on the base ofcomparative studies of the cuticules, but theyquestion the monophyly of Cupressoideae andCallitroideae and end up with intermingledgenera of both groups. It seems that Tetraclinisis best placed in the core group of Cupressoi-deae, but the position of Tetraclinis withinCupressoideae remains still problematic. WhileBRUNSFELD et al. (1994) have Tetraclinis sis-tered to Thuja and Thujopsis, it appears sis-tered to Platycladus and Microbiota in theanalyses by GADEK et al. (2000). Further stu-dies must clarify in addition, whether there areother taxa misplaced in Callitroideae or Cu-pressoideae. At present, it seems best to regardovules inserted directly at the cone axis andcontinuing the phyllotaxis of the cone scales asa special feature of reduced cones. Such reduc-tions might be expected as parallelisms, but theevidence yet available indicates that it is adevelopmental tendency restricted to the coreCupressoideae (Cupressus, Juniperus, Platy-cladus, Microbiota, Tetraclinis) and may be anapomorphy for them as well. In Cupressus andPlatycladus the transitions series probably doesnot include the extremely reduced cones withnon axillary seeds but both genera show thesame tendencies in the variation of the conemorphology as Juniperus, Tetraclinis and Mi-crobiota and therefore seem to form a welldefined monophyllum.

Acknowledgements

We are grateful to the Botanical Gardens of theUniversities of Bonn and Düsseldorf for their con-tinuous supply of material for this study. The Bo-tanic Garden of the Ruhr-University of Bochum hassupplied a lot of material for comparisons. Thegardeners of these institutions have accompaniedour studies with great interest and have frequentlypointed to unusual cones or otherwise interestingand relevant features occurring in their gymnospermcollections. The illustrations Fig. 2 and Fig. 7 havebeen supplied by Christian Schulz and PatrickKnopf who where also involved in many ways inthe practical work as well as in the fruitful discus-sions in the institute.

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Adress of the authors:

Dr. Armin Jage l , Prof. Dr. Thomas S tü tze l , Ruhr-Universität Bochum, Spezielle Botanik, Universi-tätsstraße 150, D-44780 Bochum, Germany.E-mail: [email protected]

Manuscript received: August 8th, 2003.

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