Cupressaceae Et Taxodiaceae

Home , Abies spectabilis, Agathis moorei, Araucaria laubenfelsii, Cunninghamia konishii, Plant taxonomy

AVERTISSEMENT

Ce document est le fruit d'un long travail approuvé par le jury de soutenance et mis à disposition de l'ensemble de la communauté universitaire élargie.

Il est soumis à la propriété intellectuelle de l'auteur. Ceci implique une obligation de citation et de référencement lors de l’utilisation de ce document.

D'autre part, toute contrefaçon, plagiat, reproduction illicite encourt une poursuite pénale.

Contact : [email protected]

LIENS

Code de la Propriété Intellectuelle. articles L 122. 4 Code de la Propriété Intellectuelle. articles L 335.2- L 335.10 http://www.cfcopies.com/V2/leg/leg_droi.php http://www.culture.gouv.fr/culture/infos-pratiques/droits/protection.htm

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Biogeosciences, 10, 1943–1962, 2013 Open Access www.biogeosciences.net/10/1943/2013/ doi:10.5194/bg-10-1943-2013 Biogeosciences © Author(s) 2013. CC Attribution 3.0 License.

Determination of the molecular signature of fossil conifers by experimental palaeochemotaxonomy – Part 1: The Araucariaceae family

Y. Lu, Y. Hautevelle, and R. Michels UMR 7359 CNRS Georessources, University of Lorraine, BP 239, 54506 Vandœuvre-les-Nancy` cedex, France

Correspondence to: Y. Hautevelle ([email protected])

Received: 11 July 2012 – Published in Biogeosciences Discuss.: 8 August 2012 Revised: 7 January 2013 – Accepted: 17 February 2013 – Published: 20 March 2013

Abstract. Twelve species of the conifer family Araucari- 1 Introduction aceae, including Araucaria (6 species), Agathis (3 species) and Wollemia (1 species) genera, were submitted to artifi- Numerous studies of the molecular composition of extant ter- cial maturation by confined pyrolysis. The aim of these ex- restrial plants have pointed out the chemotaxonomic values periments is to transform the biomolecules synthesized by of many biological compounds, bioterpenoids in particular these species into their homologous geomolecules in labo- (e.g. Aplin et al., 1963; Smith, 1976; Castro et al., 1996; ratory conditions. Determination of the diagenetic molecu- Mongrand et al., 2001). This means that these biomolecules lar signatures of Araucariaceae through experimentation on are synthesized by a restricted number of plant taxa and can extant representatives allows us to complete our knowledge be used as specific markers. While most bioterpenoids are in botanical palaeochemotaxonomy. Such knowledge is rele- degraded and their atomic constituents recycled in the sur- vant to palaeoenvironmental, environmental and archaeology face processes of Earth, a minor part is incorporated into purposes. All artificially diagenetic species of Araucariaceae sediments, thus joining the geological cycle. During this are firstly characterized by a predominance of saturated tetra- process, the bioterpenoids are transformed by diagenesis, cyclic diterpenoids including ent-beyerane, phyllocladanes leading to the formation of reaction products called geoter- and ent-kauranes. Moreover, Araucaria genus shows a high penoids. Their initial chemotaxonomic value can be partially relative abundance of bicyclic sesquiterpenoids, particularly or totally retained (e.g. Simoneit, 1986; Otto and Simoneit, the cadalane-type compounds accompanied by those of eu- 2001). Geoterpenoids of ancient sediments may thus provide desmane and bisabolane types as well as chamazulene and palaeochemotaxonomic information inherited from their bi- pentamethyl-dihydroindenes. Diterpenoids are of labdane, ological precursors. isopimarane and abietane types (essentially derived from abi- Botanical palaeochemotaxonomy has some specific at- etanoic acids) as well as isohexyl alkylaromatic hydrocar- tributes compared to palaeobotany and palynology in the bons. Compared to the tetracyclic diterpenoids, these com- reconstruction of palaeofloral and palaeoclimatic evolutions pounds show a relatively lower abundance, reaching trace through geological times (e.g. Vliex et al., 1994; van Aarssen levels in the case of saturated abietanes. Distributions of et al., 2000; Hautevelle et al., 2006a). Indeed, (1) plant sesquiterpenoids and diterpenoids of Agathis show some biomarkers are more widespread in the stratigraphic record similarities to that of Araucaria, with the exception of one than well-preserved plant macrofossils; (2) on the contrary to species, in which the tetracyclic compounds are absent and Palaeozoic and Mesozoic palynomorphs, they can be directly the abietane type (essentially derived from abietanoic acids) linked to specific taxa of plants, and (3) biomarkers could be predominant. High similarities between the Wollemia and readily analysed by usual organic geochemistry procedures Araucaria genera are observed. Both are characterized by on total rock samples. some high relative abundance of tetracyclic compounds with In addition to being useful to palaeofloristic and palaeocli- no predominance of other specific diterpenoids. matic studies, botanical palaeochemotaxonomy has also been recently applied in other instances. In environmental science,

Published by Copernicus Publications on behalf of the European Geosciences Union. BA2|

1944 Y. Lu et al.: Determination of the molecular signature of fossil conifers it proved to be helpful in the appreciation of past land use Pinaceae and recent anthropogenic impacts to soil (e.g, Farella et al., 2001; Heim et al., 2010; Huang et al., 2011; Lavrieux et al., Podocarpaceae Pinophyta 2011) as well as in tracing river pollution caused by paper mills (e.g. Leeming and Nichols, 1998; Wang at al., 2007). (Conifer) Araucariaceae In archaeology, palaeochemotaxonomy is used to trace di- etary habits and to understand the use of natural products in Sciadopityaceae craft and funeral rites (e.g. Colombini et al., 2005; Romanus et al., 2008). Taxaceae Most of palaeochemotaxonomic investigations are derived from published chemotaxonomic data (Otto and Wilde, Taxodiaceae 2001) and to some parts from the studies of fossil plants found in sedimentary rocks (Otto and Simoneit, 2001; Otto Cupressaceae et al., 2005; Dutta et al., 2011). Unfortunately, our knowl- Fig. 1. Phylogenetic classification of conifers. edge on botanical palaeochemotaxonomy is still very scarce. As pointed out by Hautevelle et al. (2006b), difficulties are related to the following: (1) available chemotaxonomic data 2.1 Taxonomy, geographical distribution and living (generally focused on specific biomolecules or on particu- environments lar substances, like resins or essential oils); (2) degradation and diagenetic reactions, which may significantly modify the 2.1.1 Extant Araucariaceae initial molecular fingerprint, making it difficult to perform a direct chemotaxonomic relationship between an extant plant Today, Araucariaceae species represent a dominant com- and its fossil counterpart; (3) the scarcity of reference collec- ponent of Southern Hemisphere forests. The major native tions of well-preserved and identifiable fossil plants contain- Araucariaceae species are restricted to the South American, ing organic molecules. South-West Asian and the Western Pacific regions and cover In order to fill these gaps, within the 7 extant conifer fam- a large rainfall region extending from subtropics to tropics ilies (Fig. 1), we investigated the palaeochemotaxonomy of (Enright and Hill, 1995). Nowadays, more than 40 species several extant species of the Araucariaceae (Table 1) using an are described and consist of three well-defined genera, which experimental method based on artificial maturation by con- are (1) Agathis (Salisbury, 1807), represented by 21 species, fined pyrolysis (Hautevelle et al., 2006b). This procedure al- (2) Araucaria (Jussieu, 1978) represented by 19 species and lows simulation of the conversion of biomolecules into their (3) Wollemia (Jones et al., 1995) represented by the single corresponding diagenetic geomolecules (Stankiewicz et al., species Wollemia nobilis. The latter, previously thought to 2000; Gupta et al., 2006, 2007). Aims of this study are (1) to be extinct, was rediscovered in 1994 in Australia, cloistered determine the common palaeochemotaxonomic (diagenetic) deep in the New South Wales (Jones et al., 1995). signatures of all extant Araucariaceae species, (2) to evaluate These phylogenitic relationships of Araucariaceae species the inter- and intra-generic differences within the family, (3) were also confirmed by Setoguchi et al. (1998) based on rbcL to highlight the molecular characteristics which should allow gene sequences: their distinction from other conifer families in ancient sediment samples. This contribution should serve as a database – the three genera are all monophyletic (i.e. all species for future palaeoenviroennemental, archaeological and envi- descend from a unique ancestor); ronmental research. – Araucaria could be intra-generically classified into four sections: Araucaria, Bunya, Eutacta, and Intermedia. 2 Some generalities concerning the Araucariaceae This sub-classification is in agreement with their mor- family phological characteristics (Stockey, 1982);

Araucariaceae is considered as a Southern Hemisphere – phylogenetic relationships within Agathis remain some- conifer family and was among the ﬁrst conifer families to be what unclear; individualized from their “Voltziales” ancestors during the Triassic (Stockey, 1994). Diversity and abundance of Arau- – Wollemia is the most basal extant taxon in the family, cariaceae are well preserved up to present despite some re- sharing morphologies with Araucaria and Agathis. duction of geographic distribution and extinction of several Geographic distribution of major Araucariaceae species species during evolution (Axsmith et al., 2004; Kunzmann, is given in Table 1. Extant Araucaria species develop in 2007a). the subtropical regions and extend into the marginal tropical regions where there is a lower climatic variability, while

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1945

Table 1. Phylogentic relationships, geographical range and provenance of Araucariaceae species selected for this study.

Genera Section Species Geographical range Sample’s provenance australis (D. Don) Loudon (1829) New Zealand Museum´ National Syn. : Dammara australis, Podocarpus zamiifolius (Northland & Coromandel d’Histoire Naturelle Com. : kauri, New Zealand kauri peninsulas) (Paris, France) Agathis moorei (Lindl.) Mast (1892) Botanical Garden Syn. : Dammara moorei, Dammara lanceolata New Caledonia of Lyon (France) Com. : Moore kauri robusta (C. Moore ex F. Muell.) Bailey (1883) Australia Botanical Garden Com. : Queensland kauri, smooth-bark kauri, kauri pine (Queensland) of Lyon (France) angustifolia (Bertol.) Kuntze 1898 South America Botanical Garden Syn. : A. braziliana, Columbea angustifolia (Brazil, North Argentina of Lyon (France) Com. : Parana pine, candelabra tree & Paraguay) Araucaria araucana (Molina) K. Koch (1873) South America Botanical Garden of Montet Syn. : A. imbricata (S. Chile & (Nancy, France) Com. : monkey puzzle tree SW. Argentina) bidwillii Hooker (1843) Australia Botanical Garden of the Bunya Com. : bunya, bunya pine (Queensland) Villa Thuret (France) Araucaria bernieri Buchholz 1949 Botanical Garden New Caledonia Com. : Bernier’s araucaria of Lyon (France) cunninghamii Aiton ex Lambert (1837) Australia (Queensland & Botanical Garden of Montet Com. : Hoop pine, Moreton Bay pine North of New South Wales) (Nancy, France) Eutecta heterophylla (Salisb.) Franco (1952) Syn. : A. excelsa, Dombeya excelsa, Eutassa heterophylla Norfolk Island Found in the trade Com. : Norfolk Island pine laubenfelsii Corbasson (1968) Botanical Garden South of New Caledonia Com. : De Laubenfels araucaria of Lyon (France) nemorosa de Laubenfels (1969) Botanical Garden of South of New Caledonia Com. : Boise araucaria Lyon (France) Intermedia / New Guinea Wollemia nobilis Johns, Hill and Allen (1994) Australia Wollemi Pine France Com. : Wollemi pine (Wollemi National Park) most Agathis species occupy the tropical islands (Dettmann mann, 2007b). Their distribution was then reduced during the and Clifford, 2005). These two genera, extending within the Middle Palaeocene to the Southern Hemisphere, with an ex- equatorial region of New Guinea and Southeast Asia at lower tension to the Northern Hemisphere (restricted to South-East latitude grow under a mesothermal climate, limited to the Asia). lower montane zone (Kershaw and Wagstaff, 2001). The During the Jurassic, Araucaria (especially the Eutacta and monotypic genus Wollemia is by far the most endemic genus the Bunya sections) was the first genus to appear and diver- and its few wild species (about 40 adult plants) live deep in sify. Its macrofossils and pollens broadened a wide range of a wilderness rainforest of the Wollemi National Park in New habitats in the two hemispheres (Gondwana and Laurasia), South Wales (Australia). where Jurassic climate condition was subtropical to warm- temperate (Kershaw and Wagstaff, 2001). During the Cre- 2.1.2 Fossil Araucariaceae taceous, the first effective Agathis and Wollemia fossils ap- peared, but remained restricted to Australia and New Zealand Appearance and evolution of Araucariaceae are recorded by (Hill and Bigwood, 1987; Stockey, 1994). This palaeogeo- both macrofossils and pollen in sedimentary series all around graphic limitation could have been due to the break-up of the world. The first pollen record is from the early Triassic of palaeofloristic exchanges between Gondwana and Laurasia. Australia (as ancestor) just after the Permo-Triassic extinc- Moreover, appearance of angiosperms during the Cretaceous tion, and the unequivocal Araucariaceae representatives were also forced Agathis to be more competitive (Kershaw and found in the Middle Jurassic of North Yorkshire (Stockey, Wagstaff, 2001), Wollemia probably evolved under simi- 1982; Kershaw and Wagstaff, 2001; Kunzmann, 2007b). lar circumstances. At the end of the Cretaceous, Araucaria The maximum worldwide distribution was achieved in both genus began to leave the Northern Hemisphere. As pointed hemispheres during the Cretaceous (Krassilov, 1978; Kunz- www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 BC2|

1946 Y. Lu et al.: Determination of the molecular signature of fossil conifers out by Kunzmann (2007b), their retreat from Northern Hemi- (Brophy et al., 2000). They represent the major components sphere coincides with two major events in Earth history: of araucarian essential oils (Brophy et al., 2000; Staniek (1) major changes in forest composition in Europe and North et al., 2010). Furthermore, owing to their lower molecular America, and (2) rapid environmental changes across the K- weight, these chemicals are generally highly volatile and not Pg boundary. readily preserved in sediments. Later, during the Cenozoic, Wollemia and especially Sesquiterpenoids are composed by monocyclic (e.g. ele- Agathis became more prominent from the early Eocene to the mane, germacrane and humulane types), bicyclic (e.g. cadi- early Oligocene. This development was synchronous with nane, copaane, muurolane and caryophyllane types) and tri- the diversification of angiosperms. Owing to their adaptation cyclic (e.g. aromadendrane, cubebane and gurjunane types) ability to many unfavourable conditions, such as the ultra- compounds. These chemicals are mainly represented by un- mafic soils on peridotites and the unstable climate in islands, saturated hydrocarbons, alcohols and acids, constituents of Agathis species began to colonize and diversify in New Cale- essential oil and resins (e.g. Pietsch and Konig,¨ 2000; Bro- donia and other Asia-Pacific islands (Jaffre,´ 1995). In paral- phy et al., 2000). However, they are common in conifers as lel there was a reduction of Agathis from south-eastern Aus- well as in other plants like angiosperms and bryophytes (Otto tralia due to the cooler conditions at high latitudes. Regarding and Wilde, 2001). Araucaria species, they regenerated from early Miocene un- Regarding diterpenoids, they are represented by bicyclic, der subtropical to warm-temperate conditions (Kershaw and tricyclic and tetracyclic compounds. Bicyclic diterpenoids Wagstaff, 2001). mainly composed by labdane-type compounds are common in all conifers. They are synthesized as unsaturated hydro- 2.1.3 Usefulness of Araucariaceae from the past carbons (like sclarenes and biformenes), and alcohols (like to present days sclareols) as well as acids (like agathic and communic acids) and isomers may occur (Caputo and Mangoni, 1974; Caputo The worldwide patchy and sparse distribution of Araucari- et al., 1974a, b, 1976; Thomas, 1969, Pietsch and Konig,¨ aceae in sedimentary deposits, as inferred by palaeobotanic 2000; Otto and Wilde, 2001). Other bicyclic compounds be- and palynological data, can thus provide valuable palaeo- longing to the clerodane type, like clerodadienic acids, seem climatic information. Indeed, they preferentially grow under to be restricted to two Araucaria species: A. bidwillii (Ca- warm and wet conditions, mainly in equatorial, tropical or puto and Mangoni, 1974) and A. hunsteinii (Otto and Wilde, subtropical rainforests as well as peat swamps (Kershaw and 2001). Wagstaff, 2001). Tricyclic diterpenoids reported in Araucariaceae are com- Furthermore, many Araucariaceae produce resins having posed essentially of the abietane and pimarane types. Tetra- archaeological and economical values. Agathis is highly con- cyclic diterpenoids belong to the beyerane, kaurane, phyllo- sidered as a source of attractive, straight-grained, easily cladane, trachylobane and atisane types (Brophy et al., 2000; worked timber. The wood of Agathis australis has been in- Otto and Wilde, 2001). According to Thomas (1969), Bro- tensively used in the past for the construction of canoes, phy et al. (2000) and Pietsch and Konig¨ (2000), both tri- and houses and cult objects by native Maori people of New tetracyclic diterpenoids are synthesized as unsaturated hy- Zealand. Some of these objects were well preserved and are drocarbons (like pimaradienes, abietadienes, kaurenes, etc.), of archaeological interest nowadays. The resin of Agathis acids (like abietic and isopimaric acids) and more rarely as (kauri copal, kauri gum or kauri resin) was also widely used alcohols (like phyllocladanol and phenolic abietanes, which for the manufacture of paints, varnishes and linoleum during are only reported in few Agathis species) in Araucaraiceae the XIX and XX centuries. Other Agathis living in Indonesia species. and Philippines, as Agathis dammara, produce resin having Distribution of bioterpenoids varies from one species to an important economic value (Manilla resin or Manilla co- another in fresh plants (Thomas, 1969; Brophy et al., 2000). pal). Copal has also been used for a long time in jewellery For instance, each species seems to be dominated by one and related arts. Furthermore, Araucaria may not have an or possibly two compounds. Their molecular composition equivalent economical value as Agathis, but provided wood could thus be theoretically specific to each araucarian species for ship building during several centuries. and/or genus. These data originate from a compilation of several studies, and some inconsistencies may occur. For 2.2 Chemotaxonomy instance, Thomas (1969) insists on the presence of compounds like agathic, communic, isopimaric and abietic acids Available data on the composition of monoterpenoids (C10), in Agathis species, while these compounds are not reported sesquiterpenoids (C15) and diterpenoids (C20) of many Arau- by Brophy et al. (2000). Such kinds of contradictions are cer- cariaceae representatives are here summarized. tainly due to the fact that the former studied the resins while Monoterpenoids (C10) are abundantly synthesized by the last studied essential oil. Nevertheless, chemotaxonomic Araucariaceae. Compounds, like pinene, thujene and data provide valuable knowledge to palaeochemotaxonomy. limonene are widespread in most Araucariaceae species

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1947

3 Samples and experimental procedures 3.3 Gas Chromatography-Mass Spectrometry (GC-MS) and identification of compounds 3.1 Samples Aliphatic and aromatic fractions were analysed using an HP Leaves and twigs of about 12 Araucariaceae species were se- 5890 Series II gas chromatograph coupled with an HP 5971 lected for this study, including 3 Agathis,8Araucaria and mass spectrometer (GC-MS). Polar fractions were silylated 1 Wollemia. Choice of leaves and twigs as plant material in using N, O-bis-(trimethylsilyl)trifluoroacetamide (BSTFA) ◦ this study is done based on the following reasons. (1) Most of at 60 C for 15 min before analysis. The capillary column sedimentary organic matter originating from conifers comes was a DB-5 J&W (60 m × 0.25 mm i.d., with 0.1 μm film ◦ from leaves and twigs. (2) Plant biomarkers investigated in thickness). The temperature programme was 70–315 Cat ◦ − ◦ ◦ − this paper derive from terpenoids that are of the major com- 15 C min 1 to 130 C, and then 3 C min 1 followed by an ◦ ponents of essential oils and resins. The terpenoids are trans- isothermal stage at 315 C for 15 min. Helium was the carrier − ported with resins through vessels to all part of a plant, gas (1 mL min 1 flow rate). The MS operated in the elec- including leaves and twigs. (3) Analysis of the molecular tron impact mode (EI) at 70 eV ionization energy, and mass composition of leaves and twigs provided currently available spectra were scanned from 50 to 500 Da using a quadrupole relevant chemotaxonomic and even some palaeochemotaxo- detector. Data were acquired and processed using the Agi- nomic data. More details of representatives, their phyloge- lent ChemStation software. Compounds were identified by netic relationships, native geographic distributions as well as comparison of mass spectra with the literature and library their provenances are given in the Table 1. This sampling is database (Wiley275) or by interpretation of mass spectro- believed to be well representative of the intrinsic variability metric fragmentation patterns. Relative abundance of com- of the Araucariaceae family. pounds was measured by integration of peak area.

3.2 Experimental and analytical procedures 4 Results and discussion This study focuses on the diagenetic molecular signature of Aliphatic, aromatic and polar fractions were studied for each Araucariaceae. Transformation of fresh material to its diage- Araucariaceae representative, including the extracts of fresh netic counterpart was carried out by experimental artificial plants and of their pyrolysates. Since our study mainly fo- maturation by confined pyrolysis, developed by Hautevelle cuses on palaeochemotaxonomy, the extracts of pyrolyzed et al. (2006b). Twigs and leaves of the selected plants were plants were preferentially studied. finely cut and dried under vacuum for 24 h in a desiccator ◦ at 45 C before being crushed. The plants to be pyrolysed 4.1 Molecular characteristics of artificially diagenetic were introduced into gold tubes with and without LiAlH4 Araucaria genus (Fluka No. 62420, purity 97 %, powder form). The use of LiAlH4 favours the generation of saturated over aromatic 4.1.1 Sesquiterpenoids terpanes during pyrolysis. The filled gold tubes were then sealed under an argon atmosphere and introduced into auto- Distribution of aliphatic and aromatic sesquiterpenoids of ◦ claves and heated at 280 C and 700 bars during 24 h. These Araucaria is respectively shown in Figs. 2 and 3. The pro- parameters of pyrolysis were determined to obtain the broad- portion of detected sesquiterpenoids in each representative est distribution of biomarkers (aliphatic, aromatic and polar). is given in Tables 2 and 3, which respectively correspond Biomolecules of the starting fresh plant samples of each rep- to compositions of saturated and aromatic compounds ob- resentative were also studied. tained from pyrolysis with and without LiAlH4. Di- and tri- The soluble organic compounds of fresh plants and their methylnaphthalenes are ubiquitous in each representative. ◦ pyrolysates were extracted under 80 C and 100 bars us- Araucaria species are also commonly characterized by the ing CH2Cl2 with an accelerated solvent extractor (ASE following: 350, Dionex). The total extract was then fractionated into aliphatic, aromatic and polar fractions using liquid chro- – farnesane (C15H32) and bisabolane-type compounds. matography on alumina (separation of hydrocarbon and polar Acyclic farnesane, probably derived from isomers of fraction) and silica (separation of aliphatic and aromatic frac- farnesol (trans-andcis-) detected in the fresh plants, tions from the hydrocarbon fraction) columns. The fractions is identified in all Araucaria species. Bisabolane- were successively eluted with CH2Cl2 and CH3OH/CH2Cl2 type compounds, like isomers of saturated bisabolane (50/50 v/v) on the alumina column, then with pentane, fol- (C15H30), ar-curcumene (C15H22) and dihydro-ar- lowed by pentane/CH2Cl2 (65/35 v/v) and CH3OH/CH2Cl2 curcumene (C15H24), are observed in the aliphatic (50/50 v/v) on the silica column. The obtained fractions and the aromatic fraction respectively. Ar-curcumene were diluted in hexane (4 mg mL−1 for aliphatic fraction and is often found in trace amounts for all species. 8mgmL−1 for the others) before analysis by GC-MS. Bisabolane-type compounds are generally derived from www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 C;2|

1948 Y. Lu et al.: Determination of the molecular signature of fossil conifers yoyi ihLiAlH with pyrolysis 2. Table Diterpanes Sesquiterpanes Compounds Ent type Pimarane type Abietane type Labdane Ent 16 β Cadalanes Bisabolane Eudesmane ansn 1 . . . . . 0.2 0.6 8.1 1.0 – – 6.8 3.5 212 Farnesane lrdn Fg 8b) (Fig. Clerodane byrn 7 – 274 -beyerane -16 β H-hloldns241. 29155. 923. – 39.6 19.2 59.0 1.5 22.9 – 17.6 274 (H)-phyllocladanes 2H4(i.9)24–––––––– – – – – 1.2 – – – 2.5 0.4 11.2 – – – 0.0 – – – – 9.4 45.7 – 1.9 – 51.7 – – – – 11.5 2.6 4.1 – – 5.0 – 288 8.6 274 6e) (Fig. 276 16(H)-homophyllocladane 3.8 4.8 278 278 9j) (Fig. C20H34 abietane-type Related Abietane 3 Labdane 2 Labdane 7nrhloldn Fg d 6 . – – – – – – – 1.6 260 8d) (Fig. 17-norphyllocladane 1H6(i.9)24–––––––– 2.2 – 0.3 – – – – – – 8.1 – – – Ent-16 α – – 278 264 9i) (Fig. C19H36 4 Labdane 109(208)N 109(208)N 109(208)N 109(208)N 109(208)N N bisabolane 4 α 16 α Isopimarane 9a) (Fig. C20H36 Fichtelite 1 Labdane 109(208)N N bisabolane 4 β eaieaudne % CM ekitgainnraie otehgetpa)o auae eqiepnisaddtreod nAacraeeseisotie rmthe from obtained species Araucariaceae in diterpenoids and sesquiterpenoids saturated of peak) highest the to normalized integration peak GC-MS (%, abundances Relative (H)-eudesmane (H)-edesmane H-arns24–1.7 – 274 (H)-kauranes H-274 (H)- (H) ◦ ◦ ◦ ◦ ◦ ◦ 6 5 4 3 2 1 ◦ ◦ 2 1 4 . MW 0 . . . 0.6 1.2 1.0 2.0 208 274 0 . . 0.9 0.5 0.3 0.2 1.5 0.5 – – 0.4 – 0.9 – 0.2 1.4 0.1 – 3.0 0.8 3.2 4.0 4.8 2.8 1.8 208 1.3 208 208 208 208 208 1 . . – 0.3 – – 3.6 6.6 1.3 3.8 210 210 278 7 . . . 9.6 276 7.3 276 4.8 262 4.6 278 – – – 1.5 208 nutflaAacn eneibdilicnigai eeohlaluefli nemorosa laubenfelsii heterophylla cunninghamii bidwillii bernieri Araucana Angustifolia 100 . . – 8.9 5.6 – . – 1.7 – – . – – 6.0 – – – – – – – – – 100 . 10241. 0 0 – 100 100 18.0 2.4 41.0 4.5 100 2.6 0 100 100 Arauacaria 072. – 23.7 40.7 – – (%) 56.0 50.0 86.4 6.0 2.0 2.0 – – – – – – – – – – . . 0.2 0.1 0.6 . 922.3 19.2 8.2 0.9 . . 0.3 0.2 0.9 . . 0.1 0.3 0.8 . . 0.2 0.4 3.0 . . 0.8 8.1 2.2 . . 14.6 0.0 7.5 . . – – 0.1 0.7 0.1 0.2 1.4 1.4 1.1 ––– – – – – . – 0.1 – 100 – – – – – – – – – utai orirobusta moorei australis 2154– 5.4 – – 12.1 28.1 – 13.5 – – 57.4 54.9 6.0 13.0 10.8 – 53.3 41.8 – – 10.1 100 . . 47.6 66.6 5.3 7.7 5.8 6.8 15.8 5.8 – 4.0 16.2 100 – – 6.5 – 39.7 2.4 3.5 – - 1.6 – 1.1 1.8 1.1 3.3 4.0 10.1 1.9 –– –– – –– – –– 32.2 – – –– – –– – –– – –– – –– – –– – –– Agathis 92– 49.2 (%) 100 Wollemia (%) nobilis 32.2 100 0.6 1.6 1.4 8.8 2.5 2.5 1.9 2.7 3.1 1.9 1.3 0.9 0.6 1.0 1.8 1.0 0.7 – – – – – – – – – –

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1949 – – – – – – – – – tr 50 2.7 1.7 3.4 2.6 7.4 7.7 5.7 6.5 6.9 7.8 (%) 100 27.4 14.1 18.5 14.6 19.1 21.5 12.7 18.3 26.9 33.3 11.4 13.8 20.7 17.5 15.3 16.9 19.5 nobilis Wollemia 100 20.8 (%) 8.3 12.9 100 Agathis –– – –– 18.7 13.8– – 3.3 25.4–– 15.3 3.5 1.8 5.3 4.1 – 12.8– – – 16.0 6.3 9.2 17.2 tr tr tr 4.1 –3.2 39.9 – 2.3 2.7 3.1 2.22.9 15.35.7 4.0 4.0 2.9 4.2 31.9 43.2 6.26.2 8.5 7.4 4.4 8.1 – 26.97.4 5.0 – 2.5 100 20.9 13.062.4 10.4 8.210.4 – 3.827.1 2.3 16.531.8 22.319.1 3.3 22.7 2.8 39.2 40.1 13.146.2 – 11.8 –15.9 – – – – 25.536.4 – 26.3 – –12.7 –15.8 24.1 – 12.8 – – – 9.7 43.8 25.541.5 19.2 3.2 5.5 australis moorei robusta 100 69.2 – 50.2 – 33.8 100 24.3 43.1 – 6.3 16.5 100 30.2 7.5 24.0 – 43.5 9.3 – – 40.7 16.4 1.5 – 2.1 16.2 11.7 6.9 9.0 49.5 5.7 15.6 4.1 13.9 15.38.6 4.4 51.7 3.8 33.9 19.6 1.8 100 15.8 66.6 19.8 38.0 10.2 18.4 (%) Arauacaria 100 21.9 12.1 26.8 17.8 34.8 100 56.8 33.6 66.3 –––– 100 100 Angustifolia Araucana bernieri bidwillii cunninghamii heterophylla laubenfelsii nemorosa 156 7.8 13.3 4.7 – 242 30.0 24.4 – 18.4 204 19.7 27.0 9.3 1.9 156 39.3 22.3 33.7202 – 17.0 8.3244 9.0224 5.7 39.9 28.0 – 6.6 MW 94) ◦ . 4 -curcumene -curcumene 202 tr tr tr tr tr tr tr tr Relative abundances (%, GC-MS peak integration normalized to the highest peak) of aromatic sesquiterpenoids and diterpenoids in Araucariaceae species obtained from the 19-Norabietatriene 256 28.0 – 21.1 10.7 7.3 27.5 6.6 – Tetramethyl-octahydro-naphthalene 174 – 26.3 11.3 6.2 5.8 51.3 DMN Dihydro- ar 1,3,4-trimethyl-2-(4-methylpentyl)benzene, (Fig. 5a)Calamenene 204 11.0Monoaromatic 9.2 labdane (Fig. 8a) Bis-simonellite 2.0 4.3 C18H26 (Philp, 1985, N 2,6-dimethyl-1-(4-methylpentyl)naphthalene (Fig. 5b) 240 57.3 38.3 16.7 21.9 TMNNorcadaleneCadalene 170 18-NorabietatrieneDehydroabietane1,2,3,4-tetrahydroreteneSimonellite 1849-methyl-retene 198 9.4C19H28 51.4C19H26 (Fig. 9.4 9h) 14.1 256 5.4C19H24 238 (Fig. 9f) 270 5.6Pentamethyl phenanthrene (Fig. 20.1 8c) 23.1 17.96-ethyl-2-dimethyl-1-(4-methylpentyl)naphthalene (Fig. 252 5c) 248C18H22 (Fig. 4.4 – 5d) 254 4.7 – 19.9 10.7 8.6 – 20.3 12.1 8.6 39.7 254 49.1 248 256 18.2 17.6 – – 7.7 26.3 7.1 252 11.6 8.1 14.3 – 3.0 11.9 – 4.0 33.7 19.4 9.1 20.1 33.2 31.7 – – 26.0 – 238 22.8 18.7 2.3 13.5 – 4.9 2.6 41.4 – – 48.3 47.9 7.3 41.0 9.0 29.6 82.5 – – 3.7 28.4 11.5 – 5.7 8.8 24.2 – 1.2 11.9 – 4.3 46.8 53.1 9.6 – – 83.8 12.0 22.3 – 5.4 – 65.9 – 34.7 – – 12.1 – 43.6 ar 1-methyl-10,18-bisnorabieta-8,11,13-trieneRetene 256C19H30 (Fig. 9b) 15.7C18H22 (Fig. 9c)C18H22 (Fig. 9d)C19H24 (Fig. 15.7 9e) – 28.9 234 6.3 258 8.3 238 18.8 238 29.8 252 – 23.1 18.8 49.0 – 22.3 32.4 10.9 – 43.9 – 11.6 16.3 38.4 14.8 8.4 23.3 26.5 37.3 11.4 12.5 12.4 25.2 9.5 31.3 22.2 13.9 – – 13.0 – 6.4 21.0 20.0 – CalamenePentamethyl-dihydroindene 2 188 2022-methyl-retene 24.2 15.7 9.3 5.4 4.4 48.1 13.7C19H24 (Fig. 9g) 5.1 10.0 248C19H26 25.9 (Fig. 5e) 1.3 18.2 3.5 6.2 14.6 – 8.2 252 1.7 5.0 14.1 4.3 254 – 2.2 2.3 5.5 24.1 – 5.5 11.3 8.6 – 18.5 6.0 9.7 10.8 2.3 12.1 – – 12.5 Ionene Labdane-type Isohexyl alkylaromatic hydrocarbons Pentamethyl-didydroindene 1 188 11.5 55.6 9.3 4.2 Isohexyl alkylaromatic hydrocarbons Bisabolane-type Related abietane-type n -methyl naphthalene Cadalane-type ChamazuleneAbietane-type 184 40.4 19.6 20.7 7.8 31.2 30.3 10.7 24.6 Compounds Sesquiterpenoids Diterpenoids Table 3. pyrolysis without LiAlH www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 C=2|

1950 Y. Lu et al.: Determination of the molecular signature of fossil conifers

H Araucaria angustifolia 4a Araucaria cunninghamii H * 4b 4a 4b n-C * 14 * * * * n-C 4c * 15 n-C * 4c 15 n-C * H 14 * * H ** * tr tr x tr tr

Araucaria araucana Araucaria heterophylla

* * * * x * *

Araucaria bernieri Araucaria laubenfelsii

* * * * * * x * *** * * *

Araucaria bidwillii Araucaria nemorosa

* * *

* * * * x x

retention time retention time

Fig. 2. Partial chromatograms (sesquiterpenoids retention time window) of aliphatic fraction of pyrolysates of Araucaria species. The mass ∗ spectra of 4a, 4b, and 4c are given in Fig. 4. x: absence of compound; tr: at trace level; : cadalane-type compounds.

bisabolenes found in the fresh plants. They represent sented by calamenene and calamene (C15H22, both par- one of the major class of Araucaria sesquiterpenoids tially aromatized), cadalene (C15H18, completely aro- (especially in the aliphatic fractions), except for A. matized). One norcadalene (probably the 1-isopropyl- bernieri and A. bidwillii; 7-methylnaphthalene according to the spectrum from Singh et al., 1994) is detected in all species (Fig. 4d). Its – cadalane-type compounds. They are mainly derived formation is the result of the demethylation of cadalane- from cadinol and cadinenes, which are ubiquitous in type compounds, and no more precision to its structure vascular plants. In the aliphatic fractions, a variety was proposed. In addition, cadalane-type compounds of saturated cadalane-type compounds (C15H28) are show a high abundance in most species’ samples and identiﬁed like cadinanes, muurolanes and amorphanes. represent also one of the major Araucaria sesquiter- Their spectra are commonly characterized by a molec- penoids, except for A. araucana and A.cunninghamii; ular ion at m/z 208, a low abundance (even absent) of the M+-15 ion at m/z 193, a relatively high abun- – eudesmane-type compounds. 4α(H)-eudesmane and dance of ion at m/z 165 (corresponding to the loss of 4β(H)-eudesmane are identiﬁed according to Wiley275 a isopropyl unit, M+-43) and a base peak at m/z 109 database and the spectrum published by Alexander et (corresponding to a fragmentation of A/B-ring moiety al. (1983) (Fig. 4b and 4c). The relative abundances of after the loss of precedent units) (Fig. 4a). In the aro- these two compounds vary from one species to another. matic fractions, the cadalane-type compounds are repre- It is higher in A. bernieri and at trace level in A. het-

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1951

Araucaria angustifolia Araucaria cunninghamii

4d 4f 4e 4d 4e

4f 4f 4f

Araucaria araucana Araucaria heterophylla

Araucaria bernieri Araucaria laubenfelsii

Araucaria bidwillii Araucaria nemorosa

tr tr

retention time retention time

Fig. 3. Partial chromatograms (sesquiterpenoids retention time window) of aromatic fraction of pyrolysates of Araucaria species. The mass spectra of 4d, 4e and 4f are given in Fig. 4. tr: at trace level.

erophylla as well as in A. cunninghamii. Moreover, – chamazulene (C14H16) and other compounds identiﬁed eudesmanes-type compounds are widely distributed in as pentamethyl-2,3-dihydroindenes according to their fossil vascular plants (Alexander et al., 1983). However, spectra are also remarkable in the aromatic fraction. they were not reported in the previous studies of Brophy Chamazulene elutes after cadalene and its spectrum, ac- et al. (2000) and Otto and Wilde (2001), which focus on cording to the Wiley275 database, is quite similar to fresh material; that of norcadalene, but with a molecular ion (m/z 184) more intense than its base peak at m/z 169 (Fig. 4e). ) m/z – ionene (C13H18 , with a molecular ion at 174 Due to its carbon skeleton composed of a ring com- m/z and a base peak at 159 according to Achari posed of seven carbon atoms and a pentenic ring, it et al. (1973). It was detected for most of Araucaria is probably derived from precursor of similar carbon β species. It could be derived from -carotene (like in skeleton, like aromadendrenes, alloaromadendrene and sporopollenin (which derives from some pollen exines) spathulenol, which are widespread in the fresh species (Achari et al., 1973; Simoneit, 1986). In our case, the (Brophy et al., 2000; Olawore, 2005). Pentamethyl- ionene is probably directly derived from ionone that is 2,3-dihydroindene, identiﬁed according to Wiley275 abundant in fresh plants; database, is characterized by a spectrum with a molecular ion at m/z 188 (C14H20) and a base peak at m/z 173 (M+-15) (Fig. 4f). Pentamethyl-2,3-dihydroindene and chamazulene show a higher abundance than other www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 C?2|

1952 Y. Lu et al.: Determination of the molecular signature of fossil conifers

ab109 Į H)-eudesmane 95 m/z 165

165 H 81

55 69 41 123 149 135 208 40 60 80 100 120 140 160 180 200

cd95 109 ȕ H)-eudesmane Norcadalene 169 (1-isopropyl-7-methylnaphthalene ) 81

55 69 H 184 41 123 154 137 165 193 115 141 128 161 91 105 149 177 208 51 63 69 77 84 40 60 80 100 120 140 160 180 200 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

184 e Chamazulene 169 f Pentamethyl-2,3-dihydroindene 173

153 188 127 77 92 115 128 141 77 91 115 145 158 41 51 63 70 102 51 65 84 105 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 m/z m/z

Fig. 4. Mass spectra of some identified Araucariaceae sesquiterpenoids. (a): saturated cadalane-type compounds; (b):4α(H)-eudesmane (identified using Wiley275 database); (c):4β(H)-eudesmane (identified from spectrum in Alexander et al., 1983); (d): norcadalene (identified from spectrum in Singh et al., 1994); (e): chamazulene (identified using Wiley275 database); (f): pentamethyl-2,3-dihydroindene (identified using Wiley275 database).

aromatic bicyclic sesquiterpenoids with the exception Bicyclic diterpenoids of cadalene; – furthermore, 1,3,4-trimethyl-2-(4-methylpentyl)benzene Bicyclic diterpenoids are essentially composed by labdane- (C15H24) with a molecular ion at m/z 204 and a base type compounds (C20H38). Several isomers of labdane are peak at m/z 133 was detected in all Araucaria identiﬁed in Araucaria species, although they do not show a species, but with a low abundance. According to Ellis high abundance in each representative. As shown in the lit- et al. (1996), it belongs to the family of isohexyl erature, they are generally derived from labdadiene, pheno- alkylaromatic hydrocarbons with an opened A-ring lic labdanes and communic acids present in the fresh Arau- (Fig. 5a). Its occurrence could be due to the alteration cara (Caputo and Mangoni, 1974; Caputo et al., 1974a, b, of some bicyclic compounds (like drimane) during the 1976; Otto and Wilde, 2001). Moreover, according to de pyrolysis. Paiva Campello and Fonseca, (1975), agathic acid could also be the origin of labdanes in the case of A. angustifolia. In addition, the general trend of Araucaria sesquiter- A peak having a molecular ion at m/z 244 (C18H28) is penoids, represented by the relative abundance of major class detected in the aromatic fraction in all Araucaria species. It of sesquiterpenoids in each representative, is given in Ta- shows signiﬁcant abundance in most species, but in traces ble 4. for A. bidwillii, A. laubenfelsii and A. nemorosa. According to its mass spectrum, its base peak at m/z 159 matches very 4.1.2 Diterpenoids well to fragments composed of two rings (including an aromatic ring) and two methylene units. This fragment is prob- Diterpenoids in the extracts of pyrolysates of Araucaria ably formed via the loss of a branched chain with 6 carbon species are characterized by a diversity of bicyclic, tri- atoms (Fig. 8a). This kind of fragmentation seems to be con- cyclic and tetracyclic compounds. Distributions of saturated sistent with a monoaromatic labdane. No aromatic labdane and aromatic diterpenoids are respectively shown in Figs. 6 has been described in the literature until now. and 7; the relative proportion of each diterpenoid is given in Another peak having a molecular ion at m/z 278 (C20H38) Tables 2 and 3. and a base peak at m/z 109 is detected with a low abundance in the aliphatic fraction of A. bidwillii. Its mass spectrum

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1953

a 133

m/z 133

91 119 159 204 105 145 170 55 63 77 84 187 60 80 100 120 140 160 180 200

b 169 c 183 m/z 169 m/z 183

254 169 240

153 153 224 128 141 220 41 55 77 89 105115 128 141 181 201211 41 55 65 77 91 105115 195205 40 60 80 100 120 140 160 180 200 220 240 40 60 80 100 120 140 160 180 200 220 240 260

de168 184

238 169

254 98 153 153 55 220 178 209 128 141 207 193 223 69 89 115 197 238 41 55 76 89 101 115 128 141 79 40 60 80 100 120 140 160 180 200 220 240 60 80 100 120 140 160 180 200 220 240 m/z m/z

Fig. 5. Mass spectra of identified isohexyl alkylaromatic hydrocarbons in Araucariaceae species and mass spectral cleavage patterns (identified after Ellis et al., 1996). (a): 1,3,4-trimethyl-2-(4-methylpentyl)benzene; (b): 2,6-dimethyl-1-(4-methylpentyl)- naphthalene; (c): 6-ethyl- 2-dimethyl-1-(4-methylpentyl)-naphthalenemethylretene. Mass spectra of some unidentified Araucariaceae diterpenoids, but similar to some of the identified isohexyl alkylaromatic hydrocarbons: (d) to (b) and (e) to (c).

Table 4. Major sesquiterpenoids and diterpenoids classes detected in Araucariaceae species after conﬁned pyrolysis with (saturated compounds) and without (aromatic compounds) LiAlH4 as reducing agent.

Agathis Araucaria Wollemia Class of structure australis moorei robusta angustifolia araucana bidwillii bernieri cunninghamia heterophylla laubenfelsii nemorosa nobilis Farnesane +++ ++ + +++ +++ + ++ + +++ +++ ++ ++ Bisabolane + tr tr +++ ++++ + + tr ++ ++ + + Eudesmane +++ tr tr ++ + ++ + tr tr ++++ Cadalane ++++ ++++ ++ ++++ ++ ++++ ++++ ++ +++ +++ +++ ++++ Ionene + tr tr ++tr + tr ++ tr tr tr Chamazulene ++ ++ ++ + + + ++ ++ + + + ++ ++ ++ + + + / Sesquiterpenoids Pentamethyl-dihydroindene +++++ + + + tr ++ ++ ++ + Labdane ++++++ ++ + + + + + + ++ ++ + + + + + Isohexyl alkylaromatic hydrocarbons +++ +++ + ++++ ++++ ++ +++ +++ ++++ ++ ++ ++ Abietane normal abietane (dehydroabietic acid) +++ +++++ + +++ phenolic abietane (ferruginol, sugiol tr tr tr tr tr tr tr tr tr tr tr tr and hinokiol) diagenetic abietanes ++ +++ +++ +++ tr ++++ ++++ +++ +++ +++ +++ ++++ Pimarane + // ///+ / ++++/

Diterpenoids Ent-beyerane +++ // / +++ +++ + ++ ///+ Phyllocladane ++/ + + ++ ++ tr ++++ ++++ +++ +++ / / Ent-kaurane ++++ +++ / / ++ / + + ++ ++ + + ++ + + ++ + ++++ indicates that it could also be a bicyclic compound and tives of ent-clerodadienes (Otto and Wilde, 2001) and is re- has a similar carbon skeleton to labdane. Indeed, its frag- stricted to two Araucaria species including A. bidwillii (Ca- ment at m/z 193 matches to a configuration including two puto and Mangoni, 1974; Cox et al., 2007). rings (A and B) and three methylene units, while its A/B- 2,6-dimethyl-1-(4-methylpentyl)naphthalene and 6-ethyl- ring fragment (m/z 109) contains only two methylene units. 2-dimethyl-1-(4-methylpentyl)-naphthalene are abundant for The “third” methylene unit could thus only be bound at the most species and in traces in A. launbenfelsii. These two carbon-9 position (Fig. 8b). This obtained configuration is compounds are identified from spectra published by El- consistent with a structure similar to that of clerodane. How- lis et al. (1996) and given in Fig. 5b and 5c. They be- ever, its report in extant conifers is limited to a few deriva- long to the family of isohexyl alkylaromatic hydrocarbons www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 C͚2|

1954 Y. Lu et al.: Determination of the molecular signature of fossil conifers

Araucaria angustifolia Araucaria cunninghamii

H H H

H H x 9a H H

x 8e x x

Araucaria araucana Araucaria heterophylla

H H

x x

Araucaria bernieri Araucaria laubenfelsii

H x H H H

H H 8e x 8e

x Araucaria bidwillii Araucaria nemorosa x 9a

8d x

x x x

retention time retention time

Fig. 6. Partial chromatograms (diterpenoids retention time window) of aliphatic fraction of pyrolysates of Araucaria species. The mass spectra of 8d and 8e are given in Fig. 8. The mass spectrum of 9a is given in Fig. 9. : labdanes; x: absence of compound. just like the 1,3,4-trimethyl-2-(4-methylpentyl)benzene pre- Tricyclic diterpenoid viously described. Indeed, their specific carbon skeleton with an opened A-ring could be due to some specific Few aliphatic but a high diversity of aromatic tricyclic chemical reactions, like aromatization, ring-opening pro- diterpenoids are observed. A pimarane-type compound, like cesses and rearrangement during the maturation (Ellis et isopimarane (C20H36), is detected in the aliphatic fraction al., 1996). Furthermore, the co-occurrence of 2,6-dimethyl- with a significant abundance for numerous species, like A. 1-(4-methylpentyl)naphthalene and 6-ethyl-2-dimethyl-1-(4- bernieri, A. heterophylla, A. laubenfelsii and A. nemorosa. methylpentyl)-naphthalene suggests precursors like tricyclic This kind of tricyclic aliphatic diterpenoids is probably diterpenoids (Ellis et al., 1996), for which the diagenetic derived from isopimara-7, 15-dienes, 13-isopimaradiene, products are structurally quite dissimilar to their precursors. isopimara-8(9),15-diene as well as 8β-hydroxyisopimarene, that are detected in some of the fresh Araucara species.

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1955

5b 5b 5c 5c Araucaria angustifolia Araucaria cunninghamii 5d 5d 9b 9b 8a 9e 9c 5e 9e 5e 9f 8a 9d 9c 9d 9f 9g 9g 8c 8c

Araucaria araucana Araucaria heterophylla

9b 9b 9e 9c 9d 9e 9f 9g 9f 8c

Araucaria bernieri Araucaria laubenfelsii

9c 9d 9e 9f 9g tr 9d 8c x 9e 8c

Araucaria bidwillii Araucaria nemorosa

9d 9d 9b 9g 9b 9e 9c 9e 9f tr 9f 8c 8c

retention time retention time

Fig. 7. Partial chromatograms (diterpenoids retention time window) of aromatic fractions of pyrolysates of Araucaria species. The mass spectra of 5b, 5c, 5d and 5e are given in Fig. 5. The mass spectra of 8a and 8c are given in Fig. 8. The mass spectra of 9b, 9c, 9d, 9e, 9f and 9g are given in Fig. 9. tr: in trace; x: absence of compound.

Other tricyclic diterpenoids, like abietane-type com- They may rather be consistent with a pentamethyl phenan- pounds, show a higher diversity, especially in the aro- threne. matic fraction. Related aromatic compounds are retene, dehydroabietane, 18- and 19-norabieta-8, 11, 13-trienes, tetrahydroretene, simonellite, bisnor-simonellite, 2- and 9- Tetracyclic diterpenoids methylretenes. While the saturated abietane-type compounds Tetracyclic diterpenoids, mainly ent-beyerane, 16α(H)- and like abietanes and ﬁchetelite/norabietanes are detected at 16β(H)-phyllocladanes and ent-16α(H)- and ent-16β(H)- trace level. kauranes, show relatively high abundance in each represen- These abietane-type compounds are the major diter- tative. They are identiﬁed according to the spectra published penoids of Araucaria. They are mostly derived from dehy- by Noble et al. (1985). Their spectra are all characterized droabietic acid that is observed in the polar fraction of py- by a molecular ion at m/z 274 and a base peak at m/z 123 rolysates and more generally from abietanoic acids in the (C H ). Distribution and abundance of these compounds fresh plants. Regarding the phenolic abietanes including su- 20 34 for each representative are given in Fig. 6 and Table 2. They giol, hinokiol and ferruginol (Otto and Wilde, 2001; Otto are probably derived mainly from beyerene, ent-kaurene, and Simoneit, 2001), which are known as abietane-type com- isokaurene and phylloclade-16-ene, as well as kauran-16-ol, pounds precursors for Araucariaceae as well, show a low rel- phyllocladanol and kaur-16-en-19-ol, detected in the fresh ative abundance in the fresh plants and are mostly degraded plants. Furthermore, beyerane-type compounds are detected during pyrolysis. in A. araucana, A. bidwillii and A. cunninghamii in both their A peak having a similar spectrum to those of methyl- fresh plant (beyerene) and the pyrolysates (ent-beyerane). retenes is observed in the aromatic fractions of all Araucaria Co-occurrence of phyllocladane-type and kaurane-type com- species (Fig. 8c). Compared to Alexander et al. (1995), the pounds is observed in most of Araucaria species, except of spectra of these compounds have the same molecular ion and A. angustifolia and A. nemorosa. Only phyllocladane-type or mass fragments, but are different by the fragment intensities. kaurane-type compounds are observed in A. angustifolia and in A. nemorosa respectively. www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 ͜͜2|

1956 Y. Lu et al.: Determination of the molecular signature of fossil conifers

a 159 Tentatively identified as a monoaromatic labdane

m/z 159 173

128 143 244 115 229 55 91 105 67 77 183 195 213 60 80 100 120 140 160 180 200 220 240

95 c 248 b m/z 193 Tentatively identified as m/z 109 69 109 55 a pentamethyl-phenanthrene Tentatively identified as 1 9 81 2 10 8 a clerodane 3 5 7 4 6 123 218 233 41 m/z 193 193 138 278 203 108 189 151 165 119 179 207 95 165 178 40 60 80 100 120 140 160 180 200 220 240 260 280 40 60 80 100 120 140 160 180 200 220 240

d 123 123 m/z 203 m/z 231 m/z 175 m/z 231 e Tentatively identified Tentatively identified as as a 16(H)-homo- a 17-norphyllocladane phyllocladane 95 81 69 95 245 81 m/z 273 109 109 69 m/z 123 41 55 m/z 123 260 55 41 150 288 231 135 231 175 273 137 149 163 164 259 203 189 177189 203 217 217 245 40 60 80 100 120 140 160 180 200 220 240 260 40 60 80 100 120 140 160 180 200 220 240 260 280 m/z m/z

Fig. 8. Mass spectra of some tentatively identiﬁed Araucariaceae diterpenoids and suggested mass spectral cleavage patterns for (a), (b), (d) and (e). (a): monoaromatic labdane; (b): clerodane; (c): pentamethyl-phenanthrene; (d): 17-norphyllocladane (identiﬁed according to Noble et al., 1986); (e): 16(H)-homo-phyllocladane.

A peak with a spectrum characterized by a molecular ion knowledge, still unknown. In our study, trachylobane and at m/z 260 (C19H32) with a base peak at m/z 123 is detected atiserene/isoatiserene are identified in the fresh A. araucana in A. angustifolia. This spectrum matches very well to that of and A. nemorosa, yet no possible corresponding pyrolysates 17-nortetracyclic diterpane described by Noble et al. (1986) could be identified. (Fig. 8d). Formation of this C-19 diterpane is likely due to the demethylation of a C-20 tetracyclic diterpane, while its precise molecular structure remains unclear. Furthermore, in the case of A. angustifolia, as only phyllocladanes are ob- Unidentified compounds served, the C-19 tetracyclic diterpane could rather be a 17- norphyllocladane. Numerous compounds remain unidentified in the extract Another peak, characterized by a molecular ion at m/z 288 of Araucaria pyrolysates and some of them, their mass (C21H32) and a base peak at m/z 123 is detected in A. angus- spectra are given in the Figs. 5d, 5e and 9a–h. Tenta- tifolia, A. bernieri and A. laubenfelsii (Fig. 8e). It is likely a tive identification as proposed in Fig. 9a suggests satu- methylated tetracyclic diterpane because the positive differ- rated tricyclic diterpenoid. They have, to our knowledge, ence of molecular weight of 14 Da to the well-known tetra- never been reported in previous studies on vascular plant cyclic diterpenoids corresponds to an additional CH2 group. biomarkers. Nevertheless, many of them are quite abun- This configuration is in correspondence to a C-21 tetracyclic dant in several species. For instance, it was observed that diterpane. Moreover, (1) according to the spectrum, the ion two peaks having spectra with molecular ions at m/z 238 at m/z 231 is relatively more abundant than the ions at (C18H22; Fig. 5d) and 254 (C19H26; Fig. 5e), base peaks at m/z 259; (2) A. angustifolia, A. bernieri and A. laubenfel- m/z 168 and 184, respectively, co-appear with 2,6-dimethyl- sii all show the presence of phyllocladanes. This C-21 tetra- 1-(4-methylpentyl)naphthalene and 6-ethyl-2-dimethyl-1-(4- cyclic diterpane is probably a 16(H)-homo-phyllocladane. methylpentyl)-naphthalene. These two unidentified peaks It is also interesting to point out that, according to Otto show also respectively similar abundance to 2,6-dimethyl- and Wilde (2001), tetracyclic diterpenoids like trachylobane- 1-(4-methylpentyl)naphthalene and 6-ethyl-2-dimethyl-1-(4- type and atiserane-type compounds are those exclusive to methylpentyl)-naphthalene. The relationship of the com- the Araucaria genus among all conifers. Unfortunately, the pounds is not clear; while their co-occurrence and similar diagenetic products of these two compounds are, to our fragmentation tend each couple to a similar structure. How- ever, these unidentified compounds may have some relevant

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1957

a b C20H36: ? 205 187 Tricyclic diterpane 261 C19H30: ? 55 Only for A. nemorosa & 81 95 67 A. cunninghamii 173 109

121 258 276 243 151 177 247 157 137 191 220 128 143 163 55 91 115 67 77 105 199 209 227 60 80 100 120 140 160 180 200 220 240 260 280 60 80 100 120 140 160 180 200 220 240 260 cd209 238

C18H22: ? C18H22: ?

195 - C3H7 168 179 145 238 155 179 165 193 152 223 89 119128 141 223 41 55 83 115 128 55 67 77 105 69 95 105 209 60 80 100 120 140 160 180 200 220 240 40 60 80 100 120 140 160 180 200 220 240 ef252 252 C19H24: ? C19H24: ?

182 - C5H11 195

- C4H9

165 179 165 223 195 55 152 237 69 152 55 89 115 128 208 81 95 109119 131 208 223 77 103 140 141 237 60 80 100 120 140 160 180 200 220 240 260 50 70 90 110 130 150 170 190 210 230 250

g 252 h 211 C19H24: ? C19H26: ?

209 179 - C3H7 145 254 165 194 241 131 157 171 152 115 181 197 55 89 115 128 105 223 67 77 105 141 221 237 55 67 77 91 50 70 90 110 130 150 170 190 210 230 250 50 70 90 110 130 150 170 190 210 230 250 i 109 j 259 C20H34: ? C19H36: ? Only for Norlabdane Agathis 55 163

81 95 189 69 95 274 109 55 69 123 264 81 121 177 135 150 203 245 137 151 165 179 193 245 217 231 60 80 100 120 140 160 180 200 220 240 260 60 80 100 120 140 160 180 200 220 240 260 280 m/z m/z

Fig. 9. Mass spectra of some unidentiﬁed, but recurrent Araucariaceae diterpenoids. (a) (only for A. nemorosa and A. cunninghamii in Fig. 6), (i–j) (only for Agathis, in Fig. 11): in the aliphatic fraction; (b–g) in the aromatic fraction (Figs. 6 and 11). palaeochemotaxonomic values, and special attention should ties to the molecular composition of Araucaria species are be paid to these biomarkers in future studies. observed. Farnesane, cadalane-type compounds (saturated Relative abundance of major class of Araucaria diter- cadalanes, calamene, calamenene, cadalene and norcada- penoids (including saturated and aromatic compounds) in lene), pentamethyl-dihydroindenes and chamazulene show each representative is summarized in Table 4. some high relative abundances in each Agathis representative. 1,3,4-trimethyl-2-(4-methylpentyl)benzene is detected 4.2 Molecular characteristics of artiﬁcially diagenetic as well, but at trace level. Agathis genus Furthermore, bisabolane-type compounds (bisabolanes and dihydro-ar-curcumene), which are widespread in Arau- 4.2.1 Sesquiterpenoids caria genus, are observed only in Ag. australis and show a low abundance in the other Agathis species. Concerning the The composition of sesquiterpenoids in Agathis (Ag.) eudesmanes, they are detected only in Ag. australis. species is shown in Figs. 10 (saturated) and 11 (aromatic). The proportion of each sesquiterpenoid is given in Ta- ble 2 (saturated) and Table 3 (aromatic). Some similari- www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 D;2|

1958 Y. Lu et al.: Determination of the molecular signature of fossil conifers

Aliphatic sesquiterpenoids Aromatic sesquiterpenoids

Agathis australis * Agathis australis 4a * 4b

* H 4e * 4d * n-C n-C * * 15 14 4f 4f

Agathis moorei * Agathis moorei ? *

* x * * *

* x

Agathis robusta Agathis robusta

* * * * x x

retention time retention time

Fig. 10. Partial chromatograms (sesquiterpenoids retention time windows) of aliphatic (left) and aromatic (right) fractions of pyrolysates of ∗ Agathis species. The mass spectra of 4a, 4b, 4e, 4f and 4f are given in Fig. 4. x: absence of compound ; : cadalane-type compounds.

4.2.2 Diterpenoids ally in trace in Ag. australis and Ag. moorei, but in higher abundance in Ag. robusta. As for Araucaria, the detected As sesquiterpenoids, compositions of diterpenoids of Agathis abietane-type compounds are in majority derived from de- species (Fig. 11) show also several similarities to those of hydroabietic acid (detected in the pyrolysates) as well as Araucaria. Distribution and abundance of major diterpenoids from other abietanoic acid precursors and (cetono)phenolic of the Agathis genus are given in Tables 2 and 3. abietanes (detected in the fresh plants). Only dehydroabietic Bicyclic diterpenoids are characterized by the presence of acid is observed in the pyrolysats. Tetracyclic diterpenoids, labdanes in the aliphatic fraction and monoaromatic labdane ent-beyerane is identified only in Ag. australis;16α(H)- in the aromatic fraction, which essentially originate from phyllocladane, ent-16α(H)- and ent-16β(H)- kauranes, are agathic acids (Thomas, 1969). The tricyclic diterpenoids detected in high abundance except for Ag. robusta. Despite like isopimarane is observed in Ag. australis and Ag. ro- the presence and the absence, these tetracyclic compounds busta. Isohexyl alkylaromatic hydrocarbons (2,6-dimethyl- represent the major components within the Agathis species. 1-(4-methylpentyl)naphthalene and 6-ethyl-2-dimethyl-1-(4- The unidentified compounds, like those of Fig. 8a to 8e, are methylpentyl)-naphthalene) show high relative abundance in also detected with significant abundances in Agathis species. most Agathis species and are found as traces for Ag. robusta Furthermore, some peaks show relatively high abundance (Fig. 5b and c). Abietane-type compounds show a high abun- and their spectra are respectively characterized by molecu- dance in all species. Aromatic abietanes, like retene, dehy- lar ions at m/z 264 and 274. A base peaks at m/z 109 and droabietane, 18- and 19-norabieta-8,11,13-trienes, tetrahy- 259 are observed in the aliphatic fraction of Ag. australis droretene, 2- and 9-methylretenes, are much more abundant and Ag. moorei. Their chemical formulas are, respectively, in Ag. moorei and Ag. robusta than in Ag. australis. Methyl- C20H24 and C20H34, and their spectra are given in Fig. 9i retenes and norabieta-8,11,13-trienes are detected only at and 9j. Since these spectra are neither referenced in the liter- trace level in Ag. australis. Saturated abietanes are gener- ature nor in our spectral database, their molecular structures

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1959

Aliphatic diterpenoids Aromatic diterpenoids

Agathis australis Agathis australis 5b 8a

H H

H 5c H 5d 9j H 9b

H 9i x H 5e H 9f H 9e H x H X X

Agathis moorei Agathis moorei

H 9d

H 9f 8c 9e 9f

X X

Agathis robusta Agathis robusta

9d x 9b 9f x 9e x ?

retention time retention time

Fig. 11. Partial chromatograms (diterpenoids retention time windows) of aliphatic (left) and aromatic (right) fractions of pyrolysates of Agathis species. The mass spectra of 5b to 5e are given in Fig. 5. The mass spectra of 8a and 8c are given in Fig. 8. The mass spectra of 9b to 9j are given in Fig. 9. x: absence of compound. are not yet clear. However their frequent, significant and among the sesquiterpenoids. Chamazulene, which presents a also unique presence (Fig. 9i) and predominance (Fig. 9j) relatively high abundance in both Araucaria and Agathis,is in Agathis species could be interesting for future biomarker here absent. research. Furthermore, W. nobilis shows a wide diversity of In addition, the relative abundance of major class of diterpenoids. On one hand, as the other Araucariaceae sesquiterpenoids and diterpenoids in each Agathis represen- species, it is characterized by the presence of labdane-type tative is summarized in Table 4. compounds (like labdanes), isohexyl alkylaromatic hydrocarbons (like 2,6-dimethyl-1-(4-methylpentyl)naphthalene 4.3 Molecular characteristics of artificially diagenetic and 6-ethyl-2-dimethyl-1-(4-methylpentyl)-naphthalene), of Wollemia nobilis abietane-type compounds (like retene, dehydroabietane, 18- and 19- norabieta-8,11,13-trienes, tetrahydroretene, 2- W. nobilis shows several similarities to other Araucariaceae and 9- methylretenes as well as dehydroabietic acid), and genera (Figs. 2 and 3, Figs. 6 and 7, as well as Figs. 10 tetracyclic diterpenoids (like ent-beyerane, ent-16α(H)- and and 11). Relative proportions of sesquiterpenoids and diter- ent-16β(H)- kauranes). Phyllocladane-type compounds, penoids of this monotypic genus are given in Tables 2 and 3. being largely widespread in most of Araucariaceae species, For the sesquiterpenoids, W. nobilis is characterized by are neither detected in fresh nor in pyrolysates of W. no- the presence of eudesmane-type [4α(H)- and 4β(H)- eu- bilis. Moreover, due to the high abundance of tetracyclic desmanes], bisabolane-type (bisabolane, ar-curcumene and diterpenoids, the saturated abietanes are present at trace dihydro-ar-curcumene), cadalane-type (saturated cadalanes, level in the aliphatic fraction. The unidentified compounds norcadalene, calamene, calamenene and cadalene) com- like those cited in Sect. 4.1.2. (Fig. 9) show significant pounds. Pentamethyl-dihydroindene in W. nobilis is not as abundances. The diversity of diterpenoids of W. nobilis is, abundant as those observed in Araucaria and Agathis species on the other hand, demonstrated by a great variety of other www.biogeosciences.net/10/1943/2013/ Biogeosciences, 10, 1943–1962, 2013 D=2|

1960 Y. Lu et al.: Determination of the molecular signature of fossil conifers

Sesquiterpenoids Diterpenoids a) * 4b c) * 4a * H * H H H 4c H * H * * H H * n-C15 n-C14 H

* H * H

b) d) 5b 9c 5c 5d 9d 9e 9b 8c 9g

4d 5e 9f

4f 4f

retention time retention time

Fig. 12. Partial chromatograms (sesquiterpenoids (a, b) and diterpenoids (c, d) retention time windows) of aliphatic (a, c) and aromatic (b, d) fractions of pyrolysates of Wollemia nobilis. The mass spectra of 4a, 4b, 4c, 4d and 4f are given in Fig. 4. The mass spectra of 5b to 5e ∗ are given in Fig. 5. The mass spectra of 8c are given in Fig. 8. The mass spectra of 9b to 9f are given in Fig. 9. : cadalane-type compounds. unknown aromatic diterpenoids. The particularities of these isopimarane is only detected in the Eutecta section compounds are that they are of similar abundance with no species. predominance of any specific compounds (Fig. 12). Relative abundances of major classes of sesquiterpenoids – the Agathis genus is characterized by the high abun- and diterpenoids in Wollemia nobilis are summarized in Ta- dance of sesquiterpenoids, like cadalane-type com- ble 4. pounds, chamazulene and pentamethyl-dihydroindenes. Compared to the Araucaria genus, bisabolanes and eudesmanes are occasionally present in only some species. Concerning the diterpenoids, most species are highly 5 Conclusion similar to those of Araucaria species, which are characterized by a high abundance of tetracyclic diterpanes Palaeochemotaxonomy of the Araucariaceae family is eval- and isohexyl alkylaromatic hydrocarbons, but a low uated using artificial maturation by confined pyrolysis of ex- abundance of saturated abietanes. This is the case for tant species. The Araucariaceae family is characterized by Ag. australis and Ag. moorei, but not for Ag. robusta. the remarkable predominance of saturated tetracyclic diter- The latter is characterized by the absence of tetra- penoids, including beyerane, phyllocladanes as well as kau- cyclic diterpane and a relatively lower abundance of iso- ranes. This family is also characterized by a relatively high hexyl alkylaromatic hydrocarbons. The saturated abi- abundance of sesquiterpenoids (like cadalanes, bisabolane, etanes represent thus a significant fraction of the aliphat- eudesmane as well as chamazulene) and diterpenoids (like ics. Moreover, the aromatic abietanes show constantly a abietanes). The palaeochemotaxonomy of the Araucariaceae high relative abundance in all Agathis representatives. could be summarized as follows: – Wollemia nobilis presents high similarities to Araucaria – the Araucaria genus is mainly characterized by the high genus. Presence of cadalane-types, bisabolanes, eudes- abundance of sesquiterpenoids, like eudesmanes, bis- manes, pentamethyl-dihydroindenes and also the ab- abolanes, chamazulene, pentamethyl-dihydroindenes sence of chamazulene characterize the sesquiterpenoids and more particularly by cadalane-type compounds. For signature of Wollemia nobilis. Tetracyclic compounds, the diterpenoids, saturated tetracyclic compounds are like ent-beyerane and ent-kauranes, are predominant largely predominant. Compared to the tetracyclic diter- among the diterpenoids. Other recurrent diterpenoids in penoids, other diterpenoids, like labdane, isopimarane, Araucaria and Agathis genera, like labdanes and isopi- abietanes as well as isohexyl alkylaromatic hydrocar- marane, are at trace amount or absent. The recurrent bons, show a relatively lower abundance. Moreover, abietane-type compounds are identified. The aromatic

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Y. Lu et al.: Determination of the molecular signature of fossil conifers 1961

abietanes do not seem as abundant as those observed reproduction in the Cheirolepidiaceae, J. Paleontol., 78, 402– in the two other genera. In addition, Wollemia nobilis 409, 2004. shows a great variety of unidentified aromatic diter- Brophy, J. J., Goldsack, R. J., Wu, M. Z., Fookes, C. J. R., and penoids and they are of the similar relative abundance as Forster, P. I.: The steam volatile oil of Wollemia nobilis and its much of the other well-known biomarkers like the aro- comparison with other members of the Araucariaceae (Agathis matic abietane-type compounds and the isohexyl alky- and Araucaria), Biochem. Syst. Ecol., 28, 563–578, 2000. Caputo, R. and Mangoni, L.: Diterpenes from Araucaria bidwilli, laromatic hydrocarbons. Phytochemistry, 13, 467–470, 1974. Caputo, R., Dovinola, V., and Mangoni, L.: New diterpenes from Araucaria cunninghami, Phytochemistry, 13, 475–478, 1974a. Acknowledgements. We thank Alain Rouiller, Frederic´ Lan- Caputo, R., Dovinola, V., and Mangoni, L.: New labdane diterpenes nuzel, Bastien Farre for technical assistance. We thank Fred- from Araucaria cooki, Phytochemistry 13, 471–474, 1974b. eric Thevenard´ (UMR 5276 LGLTPE, University Claude Bernard, Caputo, R., Mangoni, L., Monaco, P., Pelosi, L., and Previtera, L.: Lyon I), Anne Allaria (Botanical Garden of the Villa Thuret, Neutral diterpenes from Araucaria bidwilli, Phytochemistry, 15, INRA, Antibes), Denis Larpin (Museum Nationale d’Histoire 1401–1402, 1976. Naturelle, Paris), Romaric Pierrel and Marc Remy´ (Botanical Castro, M. A., Gordaliza, M., Miguel Del Corral, J. M., and Feli- Garden of Montet, Vandoeuvre-les-Nancy)` for their help for ciano, A. S.: The distribution of lignanoids in the order coniferae, providing samples. We also thank the Wollemi Pine France Phytochemistry, 41, 995–1011, 1996. (http://france.wollemipine.com) and the Kientzler society for Colombini, M. P., Giachi, G., Modugno, F., and Ribechini, E.: Char- providing branches of the Wollemi Pine in 2006 during the acterisation of organic residues in pottery vessels of the Roman propagation programme of this species in several botanical gardens age from Antinoe (Egypt), Microchem. J., 79, 83–90, 2005. around the world. We also wish to thank the handling editor of Cox, R. E., Yamamoto, S., Otto, A., and Simoneit, B. R. T.: Oxy- Biogeoscience (X. Wang), Dr. Sawada and a second anonymous genated di- and tricyclic diterpenoids of southern hemisphere reviewer for their appreciation, as well as for their numerous conifers, Biochem. Syst. Ecol., 35, 342–362, 2007. helpful suggestions, which improved the quality of our manuscript. de Paiva Campello, J. and Fonseca, S. F.: Diterpenes from Arau- This research benefited from the support of the Ministry of Higher caria angustifolia, Phytochemistry, 14, 2299–2300, 1975. Education and Research of France (MESR) through a PhD grant to Dettmann, M. E. and Clifford, H. T.: Biogeography of Araucari- Yueming Lu. aceae, Australia and New Zealand Forest Histories: No. 2, in: Araucarian Forests, edited by: Dargavel, J., 2, 2005. Edited by: X. Wang Dutta, S., Mallick, M., Kumar, K., Mann, U., and Greenwood, P. F.: Terpenoid composition and botanical affinity of Cretaceous resins from India and Myanmar, Int. J. Coal Geol., 85, 49–55, 2011. Ellis, L., Singh, R. K., Alexander, R., and Kagi, R. I.: Forma- tion of isohexyl alkylaromatic hydrocarbons from aromatization- rearrangement of terpenoids in the sedimentary environment: A new class of biomarker, Geochim. Cosmochim. Ac., 60, 4747– 4763, 1996. Enright, N. and Hill, R.: The southern conifers: an introduction, The publication of this article is financed by CNRS-INSU. in: Ecology of the Southern Conifers, edited by: Enright, N. and Hill, R., Melbourne University Press, Melbourne, 1–9, 1995. Farella, N., Lucotte, M., Louchouarn, P., and Roulet, M.: Deforesta- References tion modifying terrestrial organic transport in the Rio Tapajos, Brazilian Amazon, Org. Geochem., 32, 1443–1458, 2001. Achari, R. G., Shaw, G., and Holleyhead, R.: Identification of Gupta, N. S., Michels, R., Briggs, D. E. G., Evershed, R. P., and ionene and other carotenoid degradation products from the pyrol- Pancost, R. D.: The organic preservation of fossil arthropods: an ysis of sporopollenins derived from some pollen exines, a spore experimental study, P. Roy. Soc. B Biol. Sci., 273, 2777–2783, coal and the Green River shale, Chem. Geol., 12, 229–234, 1973. 2006. Alexander, R., Kagi, R., and Noble, R.: Identification of the bicyclic Gupta, N. S., Michels, R., Briggs, D. E. G., Collinson, M. E., Ev- sesquiterpenes drimane and eudesmane in petroleum, J. Chem. ershed, R. P., and Pancost, R. D.: Experimental evidence for Soc. Chem. 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&JMMJW_]ZM-# *'*"$'# ($./-4J$)L*0' * -/JMT MUJ 1) .$)# ($./-4 -$ .M( -$)# ($'*$ /4J.#$)"/*)M )) //J MMJ ($ J MMJ W_\\M # ($./-4 *! /# * *-+ S L 0/$*). *! /*/-*'M .," ,)(__J_eabN_ec]M --4J MMJ --4J MMJ 1 -.J MMJ W_^[M *'$" . .,0$/ -+ ) . *! ,3#/' /*, --#(/'L$ )/$!$/$*)J1-$/$*)) $*.4)/# .$.M"3.)" '#-.,3_aJ_ef`N_efeM $) -JMJ++' 2#$/ JMJ *#' -JMJ*' '//J MJW_\XM#-*(/*"-+#$ )'4.$.*!. *$'.M//4$ *(+*.$/$*)*!./*-*$'M )/,(&) ." ' ,#(#&" '#-.-:)# .3`fJ b^`Nb^dM $- JMMJ-.#''JMMJW_\_M/-0/0- *!#'*-!'1*)$)M )/,(&) ." " '#&)# .3^fJ _aêN_a_]M '*&#$)J M MJ !*)$)J MMJ *+*1J MMJ XVV\M *..$' 2** *! . & ,#)23&)( %'.-".%# (- .+M)*1MT$) U!-*(/# - / *0.*!/# )*-/#2 ./ -) (#/& )$).0'M& )(.)&)!#& )/,(&a]JcdeNcecM *&J MJ W_\_M # ( -$) -$..$ '*- ) '*' $./-$0/$*)M *'*"$' )/ -J )).4'1)$M *- *'*$J MJ #0&'J MMJ /#J MMJ #-(J MMJ W_^_M /0-''4 *0--$)" $) ) .M "3.)" '#-.,3_eJ_]]dN_]`dM *.(J MMJ 0)5())J MJ 19 &J MJ1) *)$%) )0-"N1)$// -/J M MMJXVWXM 1$.$*)*! /# " )0. /((#(!"'#. - T!*..$' *)$! -.UJ 2$/# .+ $' - ! - ) /* )*( )'/0- J /3*)*(4) " *'*"$'" M 0# 1) & )).(3(&3()&)!3ê_J_]N`^M - )) -J MJ W__\M 1$ ) !*- /# -'$ ./ ./" *! )"$*.+ -( +*'' ) 1*'0/$*)L +' * ,0/*-$' . /$*) !-*( .- 'J $)L 4'*-J MMJ $& 4J M MT .MUJ'*2 -$)"')/ -$"$)J1*'0/$*)) #4'*" )4M*,#(! ,J++Mf^N^^bM -$) J MJ *-)+-*./J MNMJ 'N.J MMJ $5&J MMMJ *0+ /J MJW__]MTgUN)$0'/*'J ) 2 )/N' ) -*(* $/ -+ ) !-*( /, (#*(#/&.M .," ,)( .. ,-èJ``ffN à]]M -$ 03J MJ )/4- J MJ W_][M $*.+*- . ) ($-*+')&/*) !-*( +/$)N'$) -*&. '*)" *-/*)$1 -J $./-$/*!& )5$ M/&& )&/,0(_b_J^NebM -$"".J MJ$)JMJW_[_M# ($./-4*!/# * *-+ S L*)./$/0 )/.*!/# # -/2** *!)),*/--*#./-M .," ,)(cJâ`NâaM -*+#4J M MJ*' .&JM MJ0JMMJ**& .JM MMJ*-./ -JM MJXVVVM# ./ (1*'/$' *$' *!)&& '#()#&#-) $/.*(+-$.*)2$/#*/# -( ( -.*!/# -0-$ T!."#- ) ,/,#UM#)" '#&3-. '.#-()&)!3_eJbc`NbdeM -0).! ' JM MJ*'/$.JMMJ*'/$.JMMJ &JMMJ0$))JM MJ/- )" JMMJ)& -JMMJ W__ZM #4'*" ) /$ '/$*).#$+. (*)" /# ) - *! 3* $ ) 0+- .. L 1$ ) !-*(- ,0 ) .M3-. '.#).(3^fJ_b`N_c_M

XV^MP %% 

L ($ JMMJ*3JMMJ-*!/J MMJ$ 2 ''JMJW_^YM# )*'$ $/ -+ )*$ .*!.*( * *-+.M "3.)" '#-.,3__J^^c`N^^ccM ($ JMMJ*3JMMJ$ 2 ''JMJW_^ZM# )*'$ $/ -+ )*$ .*!)),*/- ,,/!#( /-) */# -+* *-+.M"3.)" '#-.,3_`J```N``cM ($ JMMJ-)$#JMJW_]VM# ($./-4*!/# * *-+ M M$)"N(* $!$/$*). *!$ /NeJ^^J^`N/-$ )NêN*$$ M/-.,&#( )/,(&) " '#-.,3_`Jf`N^]bM ($ JMMJ) -J MMJW_\XM# ($./-4*!/# * *-+ S L*)./$/0 )/.*!/# # -/2** *!)),*/-.).,"M ))M .," ,)(êJacbNadbM +0/*J MJ *1$)*'J MJ )"*)$J MJ W_]ZM 2 $/ -+ ) . !-*( ,/,# /((#(!"'#M "3.)" '#-.,3^`JadbNadeM +0/*J MJ *1$)*'J MJ ) )"*)$J M W_]ZM 2 ' ) $/ -+ ) . !-*( ,/,# ))%#M"3.)" '#-.,3^`Jad^RadaM +0/*JMJ)"*)$J MJW_]ZM$/ -+ ) .!-*(,/,##1#&&#M"3.)" '#-.,3^`JacdNad]M +0/*JMJ)"*)$J MJ*)*JMJ '*.$J MJ- 1$/ -J MJW_]\M 0/-' $/ -+ ) .!-*( ,/,##1#&&#M"3.)" '#-.,3^bJâ]^Nâ]_M -()JMJ /#J MJW_\]M$/ -+ )*$ .M MaN+$ #4 -*$ /$$ !-*(/# *' *- .$)*! &&#.,#-)&/' &&,#-M0 ''M/-.,&#( )/,(&) " '#-.,3_]J_defN_df`M -()JMJ /#J MJW_]WM$/ -+ )*$ .M M) 2 $/ -+ )*$ $ !-*(/# *' *- .$)*! &&#.,#-)&/' &&,#-M/-.,&#( )/,(&) " '#-.,3_aJ`b`N`bfM ./-*JMMJ*- '$5JMJ$"0 ' '*--'J MMJ '$$)*JMMJW__\M# $./-$0/$*)*! '$"))*$ .$)/# *- -*)$! - M"3.)" '#-.,3a^JffbN^]^^M #'*) -JMMJW_\]M+*- .) ') N+')/ 1*'0/$*)M 0# 1) & )).(3(&3()&)!3 ^Je`Nf`M #--$;N0#0/J MJ *)))J MJ *0,0 // J MJ (J MJ -*/$)J MJ *5$:- .J MNMJ #+'J MJ '- #/J MJ XVV]M # )*+$ %-. *! ( . . L - ' 0. - 1 ' 4 (*' 0'-./0 4*!*-")$- .$ 0 .M )/,(&) ," )&)!#&# ( àJfbdNfcdM #. JMMJ*'/$.JMMJ'(./ JMMJ*-")JMJ .JM MJ$.#' -JMMJ01''JMMJ -$ J MMJ $''.J MMJ $0J MN MJ W__YM #4'*" ) /$. *! . +')/.L ) )'4.$. *! )0' */$ . ,0 ) .!-*(/# +'./$ " ) - M((&-) ." #--)/,#).(#&, ( e]Jb_eNbe]M # )"J MJ $*'.*)J MMJ -$++J MJ #2J MNMJ XVVVM #4'*" )4 *! 3 ) +#'*/3 " ) - $)! -- !-*( #'*-*+'./ (/ " ) ) )0' - - - "$*)M)& /&,"3&)! ( .#-(0)&/.#)(âJ`b`N`cbM # )"JMMJ.$JMMJW_]XM -+ ) .) ./ -*'.*!/((#(!"'#%)(#-"##M"3.)" '#-.,3 ^^J_^]eN_^]fM %% " PXV_M

# )"J MMJ 1*) 0 '*!!J MJ W_]VM 2* ) 2 $/ -+ )*$ *3$ . !-*( /# ' ! *$' *! "' 3*,#-()).%. (-#-M .," ,)( .. ,-^^J^^`^N^^`_M #*2JMN MJ- /()J MJW_\XM# # ($./-4*!/# )/0-'*- -0+- ..' .M M# ./-0/0- ) *)!$"0-/$*)*!#$)*&$*') #$)*&$*) M." '#(#(0#^cJ^_fcN ^`]]M #*2JMN MJ- /()J MJW_\XM# # ($./-4*!/# )/0-'*- -0+- ..' .MM# ./-0/0- ) *)!$"0-/$*)*!/*/-*') /*/-*'*) M." '#(#(0#^cJ^`]bN ^`^]M #-$./*+# 'J MMJ W_]YM #)*#.)*"3&&/' ( (- " )M / .+M )*1ML ) 2 *)$! - !-*( 2 ./ -)' -/M' ,#( )/,(&) ).(3c]Jc^NccM ' 'JM MJ#*(.JMMJXVV_M) )/-* 0/$*)/*+')/!*..$'.M(-$ " )$1 -.$/4- ..J 2*-&M *$!!- J MJ *( 5J MJ 1$ -*N*( 5J MJ $'# -J M MJ XVWXM $. /* *($)) *! )"$*.+ -( +$*) -. $) 0-*+ ) - / *0. )1$-*)( )/.M ,) #(!- ) ." .#)(& '3) # ( -^]fJ_]fbbN_]fbfM *'*($)$J MMJ $#$J MJ * 0")*J MJ $ #$)$J MJ XVV[M #-/ -$./$*) *! *-")$ - .$ 0 .$)+*// -41 .. '.*!/# *()" !-*()/$)* T"4+/UM#,)" '#& )/,(& dfJe`Nf]M *)))J MJ$.. )0(JMJXVVYM*)$! -/-*)/# & ') #0''+')&$)"*!/# [") $&# '#$+T .- 'Jb/# )/0-4UL$ )/$!$/$*)) *(+-$.*)2$/#)/0-'+-* 0/. ) -/ !/. (+'*4 $)*/*)./-0/$*)M )/,(&) ," )&)!#&# ( `]Jd]fNd^fM *)-)J MMJ** JMMJ-/$)JMMJ*2 J MMJ0$))JM MJ &JMMJ-$ JMMJXVVVM ) -$- '/$*).#$+.2$/#$)) /2 )/# "4()*.+ -(!($'$ . * *-+ ) #4''*' . *)))'4.$.*!/# #'*-*+'./" ) - M/-.,&#( )/,(& ) ).(3aeJd^bNd_aM **'J MMJ 0J MN MJ 1-$)J MJ W__^M *'$" / -+ )*$ . *! #$) . /*, --/- .+ $ .M #)" '#&3-. '.#-()&)!3_cJeffNf^`M *3J MMJ ((*/*J MJ //*J MJ $(*) $/J MMMJ XVV]M 34" )/ $N ) /-$4'$ $/ -+ )*$ . *! .*0/# -) # ($.+# - *)$! -.M #)" '#& 3-. '.#- ( )&)!3`bJ à_N`c_M -) JMMJW_^]M " //$*)'*). ,0 ) .*!/# )"$*.+ -( $1 -.$!$/$*)J$)L-$$.JMMJ #'*) -J MMJ -) J MM T .MUJ # *-$"$). )"$*.+ -(. ) /# $-$*'*"$' *). ,0 ) .M(-$ " )$1 -.$/4- ..J(-$ " J++M^]dNâaM -) J MMJ -$$.J MMJ -. )J MMJ W__[M # *-$"$) ) -'4 $1 -.$!$/$*) *! )"$*.+ -(.M./, `daJ_dN``M -*/ 0JMJ 0/#)JMMJ 2$.JMMJXVVVM/0-'+-* 0/.T. *) -4( /*'$/ .UJ$)L 0#))JMJ-0$.. (JMJ *) .JMT .MUJ$*# ($./-4) (*' 0'-$*'*"4*!+')/.M ( -$)*$ /4*!')/#4.$*'*"$./.*&2$''JJ++M^_b]N^`êM 0))$)"#(J MJ 4J MMJ #'.#'" -J MMJ )" )# $(J M MJ W_^YM ^` ) )'4. .*!./-0/0- J"$)") */)$'*-$"$)*!*($)$)) 3$) ( -.M "3.)" '#-.,3__JfcbNfceM

XWVMP %% 

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XW\MP %% 

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XW^MP %% 

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XXVMP %% 

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XXXMP %% 

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XXZMP %% 

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XX\MP %% 

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±Ã ±Ã Farnesanes Bisabolanes Abiétanes OH OH OH OH

COOH O HO Farnesol Farnesane Zingiberène Bisabolol Bisabolane Dihydro-ar- COOH OH HOOC curcumère ± ±± Déhydroabiétol Abiéta-8,11,13-trièn-7-one Ferruginol Sugiol Drimanes Eudesmanes 17 CH OH 15 2 20 13 1 14 1 9 10 8 7 4 4 4 H H OH H 19 18

Drimenol ͜Ƚȋ ȌǦ ͜Ⱦȋ ȌǦ ȾǦ ͘Ƚȋ ȌǦ ͘Ⱦȋ ȌǦ Abiétane Norabiétane Fichtélite Déhydroabiétane Simonellite 19-Norabiétatriène 18-Norabiétatriène 1,2,3,4-Tétrahydro Rétène rétène Cadalanes

HO H H

H H

ȽǦ ȽǦ ° ȽǦ° Cadalane Calamène Calamenène Cadalène ͕͚ǡ͕͛ǡ͕͝Ǧ± ͕͚ǡ͕͛ǡ͕͜Ǧ± 16,17-bisnor- 10-norabiéta- 10,18-Bisnorabiéta- 9-Methylrétène 2-Methylrétène 8,11,13-triène 8,11,13-triène -8,11,13-triène -8,11,13-triène déhydroabiétane

Norcadalènes Cédranes Pimaranes 16 11 13 15 20 15 17 1 16 20 11 13 14 1 9 14 10 8 8 5 10 OH 4 COOH 19 18 19 18 1-isopropyl-7-methyl- 1-isopropyl-4-methyl- 16,17,18-trisnor 16,17-Bisnordéhydro 16,17-Bisnor Cédrol ȽǦ ±° cédrane Ǧ͜ȋ͕͘Ȍǡ͕͙Ǧ° Pimarane Isopimarène Isopimarane 19-Norisopimarane naphthalène naphthalène abiétatriène abiétane simonellite Cuparanes ± Rimuanes Ȁ OH

11 OH 1 20 17 OH 8 15 5 Cuparène ɁǦ Dimethyl Trimethyl Pentamethyl Chamazulène naphtalène naphtalène ° Rimuène Rimuane 1,3,4-trimethyl-2- 2,6-dimethyl-1- 6-ethyl-2-methyl-1- 19 18 ȋ͘ǦȌ ȋ͘ǦȌ ȋ͘ǦȌ Totarol benzène naphthalène naphthalène Labdanes Béyéranes Phyllocladanes Podocarpane

11 13 11 HO 20 17 1 9 14 COOH 8 1 9 10 8 5 5 4 4

COOH 19 18 16 15 ͕͚ȋ ȌǦǦ Labdane Biformène Manool ent-béyérène ent-béyérane Phylloclad-15-ène 16Ƚȋ ȌǦ 16Ⱦȋ ȌǦ 17-norphyllocladane phyllocladane Clérodane 16 Kauranes Cembranes Isocopalane 11 OH 20 17 1 14 9 O 10 15 5 OH 4 19 18 Atisane Labdadiénol Abiénol Clérodane entǦǦ͕͚Ǧ° 16ȽǦȋ ȌǦentǦ 16Ⱦȋ ȌǦentǦ Trachylobane Cembrène Cembrane Isocopalane