ARTICLE IN PRESS

Zoologischer Anzeiger 246 (2007) 257–277 www.elsevier.de/jcz

Araucariaceae (Pinopsida): Aspects in palaeobiogeography and palaeobiodiversity in the Mesozoic$ Lutz KunzmannÃ

Museum fu¨r Mineralogie und Geologie, Staatliche Naturhistorische Sammlungen Dresden, Ko¨nigsbru¨cker Landstrasse 159, D-01109 Dresden, Germany

Received 25 January 2007; received in revised form 13 August 2007; accepted 17 August 2007 Corresponding editor: U. Fritz

Abstract

The paper examines recent information on the history of the ‘southern hemisphere’ conifer family Araucariaceae and gives supplementary notes to previously published monographs. Important data from the Mesozoic fossil record are presented and summarized to describe the ancient diversity and distribution of Araucariaceae. Information on the origin of the family and oldest fossil records of the present-day genera are assembled. Existing models on phylogenetic relationships within the family inferred from molecular data are compared with relationships between the genera determined from morphological data. Reasons for disappearance of representatives of this conifer family in the latest Cretaceous in North America and Europe are briefly discussed. r 2007 Elsevier GmbH. All rights reserved.

Keywords: Araucariaceae; Palaeobiodiversity; Palaeobiogeography; Fossil conifers; Fossil record; Mesozoic

1. Introduction heterophylla (Salisbury, 1807) Franco, 1952. Discovery of the very rare species Wollemia nobilis Jones, Hill and Araucariaceae Henkel and Hochstetter, 1865 have Allen, 1995 in the Wollemi National Park in the Blue long fascinated both botanists and palaeobotanists. Mountains, SE Australia, typify Araucariaceae again as Araucarian trees often express an unusual canopy a very distinctive and phylogenetically old family of architecture which characterizes them as ‘‘living fossils’’ conifers. Due to their today’s distribution, Araucaria- among conifers (Fig. 1). These visually striking trees are ceae are considered as a southern hemisphere family important as plantation trees in some countries and also with a typical Gondwanan relict area (e.g., Page 1990; interesting for gardening. Several species are common Enright and Hill 1995). ornamental trees all over the world, e.g., Araucaria Petrified seed cones and petrified trunks of araucarian araucana (Molina, 1782)K.Koch, 1873 and Araucaria trees are among the most beautifully preserved and most attractive plant fossils (Fig. 2). But, fossil remains of Araucariaceae are sparse and rare in the fossil record in $ Modified version of a lecture presented at the 48th Phylogenetic most parts of the world (Kershaw and Wagstaff 2001). Symposium on Historical Biogeography, Dresden, November 24–26, 2006. It is because: (1) Araucariaceae might not often have ÃTel.: +49 351 8926 406; fax: +49 351 8926 404. dominated forest vegetation in the past, (2) fossilisation E-mail address: [email protected]. of their critical organs usually needs special conditions,

0044-5231/$ - see front matter r 2007 Elsevier GmbH. All rights reserved. doi:10.1016/j.jcz.2007.08.001 ARTICLE IN PRESS 258 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Fig. 1. Araucaria araucana (Molina, 1782)K.Koch, 1873 in Andean Araucaria-Nothofagus forest, 1.200 m above sea level, near Paso Tromen, Villarrica National Park, Chile. Fig. 2. Araucaria alvarezii Dernbach and Jung, 2002 [nom. non rite publ.], petrified seed cone, Early Cretaceous, province and (3) fossil remains of Araucariaceae were recognized Chubut, Patagonia, Argentina, Palaeobotanical collection up to now generally sparse in the sediments. Palaeobo- Museum of Mineralogie and Geologie Dresden, Germany tanical studies have assigned Araucariaceae as the most (MMG PB SAK 53:1). ‘basal’ among the extant conifer families. They appear to have been distinctive since at least the Late Triassic (Stockey 1994) nested within the Voltziales. In the 2. Extant representatives and their distribution Mesozoic, they show a bi-hemisphere distributional areas pattern with records in Gondwana and Laurasia. Fossil evidence suggests that from the Cretaceous-Palaeogene Araucariaceae form a distinctive family of conifers boundary to present, the family has gradually declined without very close affinities to other living families in number of taxa and geographic distribution (Taylor (Page 1990). Phylogenetically, Araucariaceae are sister and Taylor 1993). Araucariaceae disappeared in the to Podocarpaceae (including Phyllocladaceae); both latest Cretaceous from the palaeovegetation in most forming the sister group of Cupressaceae s. l., Taxaceae, parts of the northern hemisphere. Cephalotaxaceae and Sciadopityaceae (Stefanovic´et al. Much of the former work on fossil Araucariaceae 1998). This is also clearly indicated by different seed was summarized by Stockey (1982, 1994). Enright and cone morphologies (Farjon 2001, 2005). Araucariaceae Hill (1995) and Kershaw and Wagstaff (2001) have and Podocarpaceae as typical ‘southern hemisphere’ focused on southern hemisphere records in their families share a common ancestry from many points of comprehensive treatises. An annotated compendium view (Miller 1988). on published records is edited by Dijkstra et al. (1999). Living Araucariaceae consist of the three well- The present paper gives an updated state of the art with established genera Agathis Salisbury, 1807, Araucaria special consideration of European fossil data from the Jussieu, 1789 and Wollemia Jones, Hill and Allen, 1995, Mesozoic. numbering 41 species and one variety (Farjon 2001). ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 259

Fig. 3. Recent distribution of Agathis Salisbury, 1807 (compiled from Farjon 2001; Enright and Hill 1995).

Agathis is mostly distributed in the ecozones of free part of the ovuliferous scale, and free seeds with two Indomalaya and Australasia (Fig. 3) with two relatively marginal asymmetrically developed wings. Cone scales diverse regions in Borneo (5 spp., 4 endemic) and in and seeds are shed separately at maturity. Cuticular New Caledonia (5 spp., all endemic). In all other regions micromorphology of Agathis leaves is characterized by not more than two species occur (Farjon 2001). Much of stomata with Florin rings (Stockey 1993). Species of its distribution area covers the Malesian botanical Agathis are monoecious. province (Malay Peninsula, Sumatra, Borneo, Philip- In contrast, Araucaria has a disjunct distribution with pines, New Guinea) which straddles the boundary most species occurring in the Australasian ecozone between Indomalaya and Australasia. Agathis may be (Australia, New Guinea, New Caledonia, Norfolk called the ‘most tropical’ among present-day conifer Island) too, but two species are distributed in South genera concentrated in montane tropical to subtropical America (Fig. 4). This disjunction is a characteristic rainforests. Only Agathis australis occurs in warm- feature of Gondwanan relict elements. New Caledonia is temperate humid rainforest in northern New Zealand. the most diverse region with 13 Araucaria species of the Agathis shows relatively small interspecific differences 19 known species. All 13 are endemic to the islands amongst the extant 21 species. A subdivision into (Farjon 2001) and belong to the section Eutacta. Most sections, like in Araucaria, is far from being settled. of these species are adapted to ultramafic rocks and their Most of the species occur as scattered trees or as small derived soils (Jaffre´1995). Therefore it is suggested that groves within dense rainforests, usually as canopy there was a remarkable differentiation of new species emergents (Page 1990). In New Caledonia species nested in section Eutacta after the emplacement of the are limited mostly to maquis on ultramafic soils ultramafic rocks in the late Eocene (40–45 myr, Jaffre´ (Farjon 2001). The individual ecological and social 1995). In all other regions Araucaria has only one or two status of all Agathis species has been discussed in species (Farjon 2001). Ecological amplitude of Araucar- Whitmore and Page (1980) and in Enright and Hill ia is clearly wider than in Agathis. Araucaria occurs in (1995). Agathis is distinguished by petiolate leaves montane tropical to subtropical rainforests in Malesia, without a conspicuous midrib in opposite to suboppo- in maquis in New Caledonia and in temperate to cool site arrangement, wedge-shaped cone scales without any temperate mixed conifer–angiosperm forests up to the ARTICLE IN PRESS 260 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Fig. 4. Recent distribution of Araucaria Jussieu, 1789 (compiled from Farjon 2001; Enright and Hill 1995).

timber line in the Andes in South America (Enright and Hill 1995). Araucaria shows relatively large interspecific differences amongst its extant 19 species. A subdivision into the four sections Araucaria, Bunya Wilde and Eames, 1952, Eutacta Endlicher, 1842 and Intermedia White, 1947 has been accepted widely. Most of the species occur as small groves or as local pure popula- tions in more mesic temperate habitats on tropical mountain flanks. They are usually canopy emergents (Page 1990). The individual ecological and social status of all Araucaria species has been discussed in Enright and Hill (1995). Araucaria is distinguished by non-petiolate spirally arranged leaves, cone scales with free ovuliferous tips Fig. 5. Recent distribution of Wollemia Jones et al., 1995. (ligulae) and large adnate seeds which are fused to the scale. Cone scales and seeds are shed as a complex at moist, fire-proof nature along a permanent small stream maturity. Cuticular micromorphology of Araucaria in the bottom of a canyon (Enright and Hill 1995). The leaves is characterized by stomata without Florin rings local climate is described as warm-temperate rainforest (Stockey 1993). Most of the Araucaria species are micro-environment (Heady et al. 2002). On the basis of dioecious (Page 1990). seed cone morphology Wollemia is closer related to The monotypic genus Wollemia, recently discovered Agathis than to Araucaria (Jones et al. 1995). Wollemia in a deep sandstone gorge in the Blue Mountains is easily distinguished by pollen from Agathis and Wollemi National Park, New South Wales, Australia Araucaria. The wood does not show major distinctive (Fig. 5), is distinguished by trimorphic leaves in features (Heady et al. 2002). This accords with previous distichous and tetrastichous arrangement, wedge-shaped studies in wood of extant Araucariaceae, suggesting that cone scales without free ovuliferous parts and circum- it is impossible to distinguish genera based on wood. ferentially winged seeds which are shed free from the Phylogenetic relationships within the family based on scale at maturity (Jones et al. 1995). The small morphological concepts are well established, providing population consists of approximately 40 adult trees. evidence that Wollemia is more closely related to Agathis Autecology of W. nobilis is characterized by a very than to Araucaria. In contrast, Setoguchi et al. (1998) ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 261

Fig. 6. Phylogenetic relationships within Araucariaceae inferred from matK and rbcL data, ML GTR plus G model, bootstrap support from 100 replicates (S. Renner, in litt. 2006). Materials: Agathis borneensis: rbcL data Chaw et al. (2000), matK data Cheng et al. (2000); Agathis robusta: rbcL data Conran et al. (2000), matK data Quinn et al. (2002); Agathis vitiensis: rbcL data Setoguchi et al. (1998), matK data Quinn et al. (2002); Araucaria araucana: rbcL data Conran et al. (2000), matK data Hilu et al. (unpubl.); Araucaria heterophylla: rbcL data Setoguchi et al. (1998), matK data Quinn et al. (2002); Araucaria hunsteinii: rbcL data Setoguchi et al. (1998), matK data Quinn et al. (2002); Wollemia nobilis: rbcL data Gilmore and Hill (1997), matK data Quinn et al. (2002). A: most recent common ancestor of Agathis and Wollemia: 112 myr, based on fossil data: oldest Agathis leaves: Albian (Cantrill 1992), oldest Wollemia (Dilwynites) pollen: Turonian (Chambers et al. 1998), oldest Wollemia-like cone scales: late Albian (Cantrill and Falcon-Lang 2001). published a molecular tree based on rbCL sequence data group of 13 Araucaria species endemic in New suggesting Agathis+Araucaria as sister of Wollemia. Caledonia. Unfortunately, this tree has been widely accepted by palaeobotanists and commonly cited when discussing phylogeny of the family and relationships of extinct 3. Fossil record – a mosaic of ‘organ-taxa’ and representatives (e.g., Kershaw and Wagstaff 2001; names Cantrill and Raine 2006). Different results from an analysis based on 28S rRNA gene sequences strongly The fossil record of Araucariaceae, and of other support Wollemia being sister to Agathis (Stefanovic´ woody plants too, presents a mosaic of dispersed organs et al. 1998), corresponding with morphological data. (stems, seed cones, pollen cones, seeds, pollen, foliage This result is part of a wider phylogenetic analysis of all shoots, etc.). Whenever possible fossil specimens will be living conifer families by Stefanovic´et al. (1998) using described as fossil species (morpho-species) using the only six selected species of Araucariaceae. Herein a ‘whole-plant concept’ and they will be placed into extant cladogram based on rbcL+matK sequence data from or extinct genera and other taxonomic categories. In selected species is presented (Fig. 6, S. Renner, in litt. many cases isolated organs are placed in ‘organ-genera’ 2006). This Renner tree corroborates the data by that cannot reliably be assigned to a single extant or Stefanovic´et al. (1998) and Jones et al. (1995) in that extinct genus. They may be assigned, however, to a Wollemia is revealed as sister taxon of Agathis while family. That makes investigations in palaeobiodiversity Araucaria as sister to Agathis+Wollemia. within a certain family and palaeobiogeography of Nevertheless, Setoguchi et al. (1998) have published certain taxa particularly problematic. the first molecular cladogram based on data from most Concerning fossil Araucariaceae, the present of the extant Araucariaceae species. It is quite interest- knowledge is herein summarized briefly. Most of well- ing that this cladogram partly fits very well to the preserved fossil seed cones or seed cone scale complexes morphological data, e.g., different interspecific varia- can be placed into extant genera. So far, only one extinct bility in Agathis and in Araucaria; definition of sections seed cone genus that differs significantly from the extant within Araucaria; low genetic variability within the ones has been discovered and described. Wairarapaia ARTICLE IN PRESS 262 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 mildenhallii Cantrill and Raine, 2006 from the Cretac- and Philippe (2001) regarded the generic character eous (Albian-Cenomanian) of New Zealand is morpho- ‘‘Randzellen’’ of Dammaroxylon as intercellular spaces logically distinct from all three extant genera but seems that occur in various wood types, both extinct and to be related to Wollemia (Cantrill and Raine 2006). If extant. They treated Dammaroxylon as synonym of seed cones and/or isolated seed cone scales cannot be Agathoxylon. Thus, the fossil record of Agathoxylon placed into an extant genus the morphotaxon Araucar- indicates only the occurrence of the crown Araucar- ites C. Presl in Sternberg, 1838 is commonly used, iaceae itself. although this name is ambiguous. Zijlstra and van Additional extinct wood morphotypes are also Konijnenburg-van Cittert (2000) proposed the conser- known. Bamford and Philippe (2001) consider Araucar- vation of Araucarites C. Presl against Araucarites Endl. iopitys Jeffrey in Hollick and Jeffrey, 1909 as a distinct (fossil trunk of Carboniferous conifers, no species name fossil araucariaceous wood type that shows ‘presence of given, no locality) to confirm the established usage for thickenings on the tangential wall of ray cells’. These araucariaceous female cones and cone scales, but did not thickenings are absent in Agathoxylon. Other extinct mention Kvacˇek (1971) who re-determined the type genera like Araucariodendron Krassilov, 1965 are in specimen as affinis Pinus L. This badly preserved seed need of modern revision. However, this indicates the cone from the latest Late Eocene of Ha¨ring (Austria) existence of clearly distinct wood types in fossil was previously referred to Doliostrobus taxiformis Araucariaceae and therefore perhaps a higher diversity (Sternberg, 1833) Kvacˇek, 1971. The latter determina- of the family in the past. tions may completely rule out the usage of Araucarites The existence of extinct genera is probably demon- for fossil Araucariaceae. strated also by a variety of pollen morpho-genera in the For poorly preserved cone material the morpho-genus Mesozoic. Araucariacites Cookson ex Couper, 1953, Araucariostrobus Krasser, 1921 is available. Araucarios- Balmeiopsis Archangelsky, 1979 (Archangelsky 1994; trobus indicates strong affinities of a fossil specimen to Batten and Dutta 1997), Cyclusphaera Elsik, 1966 the Araucariaceae, independently whether the specimen (del Fueyo and Archangelsky 2005)andDilwynites may represent a seed cone or pollen cone. Harris, 1965 (Chambers et al. 1998) are pollen morph- Fossil wood of the family is usually assigned to the genera derived from fossil representatives of the morpho-genus Araucarioxylon Krauss in Schimper, family. Callialasporites Sukh-Dev, 1961 is treated as 1870 (as ‘Araucaroxylon’) [nom. ill. et superfluous; araucarian type by van Konijnenburg-van Cittert e.g., Bamford and Philippe 2001]. This procedure is (1971) and by Batten and Dutta (1997) and as podocarp highly problematic not only from a nomenclatural point by Archangelsky (1994). Araucariacites is considered of view. Due to the rules of the ICBN (Greuter 2000), as taxon for pollen of both fossil Araucaria and Agathoxylon Hartig, 1848 has priority and the name fossil Agathis (Stockey 1994), because it is difficult, or Araucarioxylon is a synonym to Pinites Lindley and at the moment impossible, to distinguish between Hutton, 1832 ¼ Dadoxylon Endlicher, 1847 (Bamford present-day Araucaria and Agathis based on pollen. and Philippe 2001). However, araucarioid wood types Pollen of Wollemia is distinct and it has been shown were produced by a wide array of late Palaeozoic and that the long-known fossil type Dilwynites represents Mesozoic gymnosperms including glossopteridalean, Wollemia (Chambers et al. 1998). Furthermore, pentoxylalean plants and other groups (Stewart and several pollen morpho-genera clearly show a derivation Rothwell 1993). They have been described under a from Araucariaceae, but their generic affinities are couple of morpho-genera that often differ only in a few unknown. They have been found partly inside of xylotomical features. That makes often the decision pollen cones or isolated microsporangia (e.g., Barale complicated whether a fossil specimen is a representative 1992; del Fueyo and Archangelsky 2005). Araucariacites of the Araucariaceae or not. europaeus Krutzsch, 1971 from the European Paleogene Generally, it is not possible to separate wood of the is most likely the pollen of the extinct conifer present-day genera on the basis of xylotomical features Doliostrobus taxiformis (Sternberg, 1833) Kvacˇek, usually described using LM and SEM (Stockey 1994; 1971 (Z. Kvacˇek 2002). Its phylogenetic relationship Heady et al. 2002). For the first time Schultze-Motel to Araucariaceae has been often discussed (e.g., (1966) has referred to the problem of the botanical Kunzmann 1999). Recently the quite distinct combina- affinity of Cretaceous wood with araucarioid crossfield tion of morphological characters of Doliostrobus Mar- pitting. He pointed out that there is no obvious criterion ion, 1888 was emphasized by Z. Kvacˇek (2002) who to distinguish between wood of extant Araucaria and established subsequently the new extinct conifer family Agathis even if the SEM is used. Dammaroxylon Doliostrobaceae Z. Kvacˇek, 2002. Schultze-Motel, 1966 is considered as a morpho-genus Finally, the identification of foliage shoots as of fossil Araucariaceae with botanical affinities both to representatives of Araucariaceae is highly problematic Araucaria and Agathis. Schultze-Motel (1966) treated if the shoots are not attached to fertile organs. Sterile Agathoxylon as ‘‘genus dubium’’. Later, Bamford vegetative shoots are identified as araucarioid only by ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 263

Fig. 7. Brachyphyllum obesum Heer, 1881, foliage shoot and cuticle micromorphology of leaves, Araripe basin, Brazil, Late Aptian Crato Formation, Palaeobotanical collection Museum of Natural History of the Humboldt University Berlin, Germany (from Kunzmann et al. 2004). (A) Shoot showing three orders of branching, MB PB 1999/452 (scale bar: 9 cm); (B) abaxial leaf cuticle by LM, MB PB LM 1999/468-1 (scale bar: 1 cm); (C) abaxial leaf cuticle with stomata by SEM, MB PB SEM 1999/468-2 (scale bar: 50 mm). cell structures of the leaf epidermis obtained from Hutton, 1836; Harris 1979; Brachyphyllum obesum Heer, cuticles (cuticle micromorphology sensu Stockey 1993). 1881; Kunzmann et al. 2004; Fig. 7). Cuticle micromorphology, especially of the stomata, is Based on the diversity of araucarian ‘organ-genera’ it essential to get generic characters to distinguish extant is argued that the Araucariaceae had a significantly genera (Stockey 1994). The morpho-genus Araucarioides higher generic diversity in the Mesozoic than today. This Bigwood and Hill, 1985 from the Eocene of Tasmania is hardly proved by extinct morpho-types of fertile combines morphological and cuticular features of organs. One should also remember a basic principle in Agathis and Araucaria, suggesting the presence of an Palaeontology that says that the fossil record shows only extinct araucarian genus. More recently Hill (1995) a fraction of the original diversity in the past. considered Araucarioides as fossil leaf morpho-type of Wollemia. The fossil record yields specimens that clearly show morphological affinities to Araucariaceae. However, 4. Origin and distribution in the Triassic cuticle micromorphology, although being typical arau- carioid, and leaf shape are distinct from extant species. Conifers with one-seeded cone scale complexes Dammarophyllum (Velenovsky´, 1889) Velenovsky´ in (Araucariaceae, Podocarpaceae, Taxaceae) may have J. Kvacˇek, 2003, Dammarites C. Presl in Sternberg, derived from voltzialean conifers in the latest Permian 1838 and Lindleycladus Harris, 1979 belong to the first or early Triassic, especially from Ullmanniaceae Zim- group with morphological affinities to Agathis, but mermann, 1959 and allied groups (e.g., Stewart and different phyllotaxis and cuticle micromorphology. Rothwell 1993). Voltzialean conifers occurred in both They might be representatives of totally different extinct hemispheres in the Triassic (e.g., Hermsen et al. 2007; conifer families (J.H.A. van Konijnenburg-van Cittert, Taylor and Taylor 1993). In Ullmannia Goeppert, 1850 pers. comm. 2006). On the other hand, it is known that the seed cone consists of flattened ovuliferous short certain species of the Mesozoic morpho-genera Brachy- shoots with the individual scales fused together, forming phyllum Lindley and Hutton, 1836 emend. Harris, 1979 a fertile scale like in extant conifers which is free from and Pagiophyllum Heer, 1881 emend. Harris, 1979 the subtending bract. The fertile scale bears a single belong to the Araucariaceae, based on cuticle micro- inverted ovule/seed on the adaxial side. Modern conifer morphology (e.g., Brachyphyllum mamillare Lindley and families like Araucariaceae probably evolved in the ARTICLE IN PRESS 264 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Fig. 8. Selected fossil records of Araucariaceae in the Triassic showing nearly worldwide distribution, plotted in a simplified palaeogeographic map of the Late Triassic in rectangular format (modified after Blakey 2005). (1) Araucarioid pollen grains, Early Triassic, Australia (de Jersey 1968); (2) Araucariacites sp., Middle to Late Triassic, Argentina (Ottone et al. 2005); (3) Agathoxylon cordaianum, Late Triassic, Germany (Hartig 1848; Bamford and Philippe 2001); (4) Araucarioxylon arizonicum, Late Triassic, USA (Wright 2002); (5) Agathoxylon sp., Late Triassic, Brazil (Pires and Guerra-Sommer 2004), Araucarioxylon sp., Late Triassic, Brazil (Minello 1994); (6) Agathoxylon sp., Late Triassic, Korea (Kim et al. 2005); (7) Araucarites parsorensis , Late Triassic, India (Lele 1956; McLoughlini et al. 1997); for more detailed information see Section 4.

Early Triassic after the major extinction phase at the lales and among other conifers such as Cheirolepidiaceae Permian–Triassic boundary. But, the origin of the (e.g., Stewart and Rothwell 1993). Thus, all Triassic Araucariaceae is far from being settled (Taylor and records of araucaroid wood are not conclusively fossil Taylor 1993). evidence for Araucariaceae. It is still difficult to The early record of the family consisting of wood, distinguish between araucarioid wood of voltzialean seed cone scales and pollen (Fig. 8) is characterized by conifers from the Late Carboniferous and Permian several uncertainties. The earliest find is pollen from the (morpho-genus Pinites) and wood of Mesozoic Araucar- Early Triassic of Australia putatively attributable to the iaceae. As mentioned above, the situation is more family (de Jersey 1968). Pollen of the Araucariacites type complicated by many illegitimate and superfluous names is reported from the Middle to Late Triassic Los Rastros as Araucarioxylon [nom. ill.] or Dadoxylon [nom. Formation in central-western Argentina (Ottone et al. superfl.]. Nevertheless, many true records of wood of 2005). fossil Araucariaceae have been published under the The earliest find of araucarian seed cone scales comes names of Agathoxylon, Araucarioxylon or Dadoxylon, from the Gondwanan Parsora flora of India. Araucarites e.g., the type species Agathoxylon cordaianum Hartig, parsorensis Lele, 1956 unambiguously represents a fossil 1848 from the Triassic of Coburg, Germany (Bamford Araucariaceae. Recently the stratigraphic age of the and Philippe 2001) and Araucarioxylon arizonicum Parsora Formation is considered as Late Triassic Knowlton, 1888 from the Late Triassic Chinle Forma- (McLoughlini et al. 1997). tion, Arizona, USA (Wright 2002). In that time Arizona Much of the wood record is difficult to interpret and was at 151N palaeolatitude and the palaeoclimate was to verify because of the number of Permian and Triassic characterized by tropical to subtropical conditions with conifers with superficially similar araucarioid secondary saisonal monsunal-like precipitation (Wright 2002). Be- wood and the proliferation of generic names used to side wood fossils from North America and Europe there describe them. There is a nearly worldwide Triassic is also evidence from other continents, e.g., from South record of araucarioid wood which is often named America: Agathoxylon sp. (Pires and Guerra-Sommer Araucarioxylon [nom. ill.]. But, several Late Palaeozoic 2004) and Araucarioxylon sp. (Minello 1994) from the and Mesozoic tracheidoxyls with araucarioid cross fields Late Triassic petrified forest of Sa˜o Pedro do Sul, are available to designate araucaroid wood types Caturrita Formation, Parana´ Basin, province Rio (Philippe 1993; Bamford and Philippe 2001). Not all of Grande do Sul, Brazil, and from Asia: Agathoxylon sp. them are considered as representatives of the Araucar- in Late Triassic of NE China, Korea, Japan (Kim et al. iaceae, some may belong to voltzialean conifers. In the 2005; Philippe et al. 2006). Various records of so-called southern hemisphere wood with araucarioid characters Araucarioxylon in S African petrified forests (Namibia, has been found also among Glossopteridales, Pentoxy- Zimbabwe) and in N Madagascar are in need of revision. ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 265

These fossil wood, seed cone scale and pollen records (Fig. 9), the southern Gondwana (todays South really suggest a worldwide distribution of Araucariaceae America, Africa, Madagascar, India, Antactica, Aus- in the Late Triassic (Fig. 8). Selected records are plotted tralia) and the northern Lausasia (North America, in a modified version of a rectangular palaeogeographic Europe, most of Asia). map of the Late Triassic published online by Blakey Fossil representatives are been identified from nearly (2005). The palaeogeographic situation in the Late all parts of Gondwana (Fig. 9). Well known are the Triassic is characterized by the ongoing existence of beautifully and excellently preserved remains from the the Late Palaeozoic Pangaea super-continent. Laurasia Middle Jurassic Cerro Madre e Hija (Cerro Cuadrado) in the northern hemisphere is still connected with the Petrified Forest, Matilde Formation in Patagonia, southern continent Gondwana but partly separated by Argentina. Petrified trunks (Agathoxylon matildense the Tethys Ocean (Fig. 8). Breakup of Gondwana Zamuner and Falaschi, 2005), seed cones (Araucaria started in the Jurassic. A nearly worldwide distribution mirabilis (Spegazzini, 1924) Windhausen, 1931; Stockey of Araucariaceae even in the Late Triassic was 1978), foliage shoots and ‘seedlings’ (Stockey 2002a) can supported by the Pangaea situation. be used to reconstruct a fossil species following the ‘whole-plant concept’. The seed cone morphology of A. mirabilis indicates botanical affinities to the extant Araucaria bidwillii, a species of the section Bunya 5. Diversification in the Jurassic (Hernandez-Castillo and Stockey 2002). Cones belonging to the fossil morpho-species Arau- An ongoing nearly worldwide distribution of Arau- carites bindrabunensis Vishnu-Mittre, 1954 from the cariaceae in the Jurassic is indicated by the fossil record. Rajmahal Hills, India may be also related to extant However, they increased in abundance and diversity A. bidwillii of the section Bunya (Hernandez-Castillo during the Jurassic. Araucariaceae have occupied a wide and Stockey 2002). From the same area Singh (1956) range of habitats and due to subtropical to warm- described isolated seed-cone scales as Araucarites temperate conditions in mid-latitudes they are con- nipaniensis. stantly at about 501N(Krassilov 1978). Jurassic Foliage of Araucaria africana Krassilov, 1978 landmasses have been divided into two huge continents is described from the In-Eserin borehole in the

Fig. 9. Selected fossil records of Araucariaceae in the Jurassic showing a nearly worldwide distribution, plotted in a simplified palaeogeographic map of the mid-Jurassic in rectangular format (modified after Blakey 2005). (1) Araucarioxylon sp., Early and Middle Jurassic, England (Morgans 1999), Araucaria sphaerocarpa, Middle Jurassic, England (Stockey 1980a), Araucarites phillipsii, Middle Jurassic, England (Harris 1979), Araucaria brownii, Late Jurassic, England (Stockey 1980b); (2) Araucarites haeberleinii, Late Jurassic, Germany (Jung 1996); (3) Araucaria moreauana, Late Jurassic, France (Barale 1981); (4) Araucaria sp., Late Jurassic, USA (Gee 2006); (5) Araucaria africana, Late Jurassic, Mali/Niger (Krassilov 1978); (6) Araucariacites and Balmeiopsis, Late Jurassic to earliest Cretaceous, Sudan/Egypt (Kedves and Pa´rdutz 1974); (7) Agathoxylon liguaensis, Early Jurassic, Chile (Torres and Philippe 2002); (8) Araucaria mirabilis, Middle Jurassic, Argentina (Stockey 1978), Agathoxylon matildense, Middle Jurassic, Argentina (Zamuner and Falaschi 2005); (9) Araucarites bindrabunensis, Jurassic, India (Vishnu-Mittre 1954); (10) Araucariaceae pollen, Early, Middle and Late Jurassic, Australia (Kershaw and Wagstaff 2001); (11) Callialasporites sp., Jurassic, Antarctica (Townrow 1967), ‘primitive forms of Araucariaceae’, Jurassic, Antarctica (Dutra and Rockenbach Boardman 2006); for more detailed information see chapter 5. ARTICLE IN PRESS 266 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Mali-Nigerian basin, Africa, being the main component 2002b). Thus, most of the worldwide Jurassic record of a lowland araucarian forest (Krassilov 1978). represents probably not fossil species of Araucaria but Araucarioid pollen of Araucariacites and Balmeiopsis species of a stem group of the family. Nevertheless, types has been found in the Jurassic-Cretaceous Nubia species of the genus Araucaria nested within this Formation in Africa (Kedves and Pa´rdutz 1974). ‘generalized’ araucarian type or stem Araucariaceae Araucarian cones were mentioned from the Upper may have evolved during mid to Late Jurassic probably Jurassic of Madagascar (Barale et al. 1988) and from the earlier than species of the other extant genera. Sahara region (Krassilov 1977). Some of these above-mentioned morpho-species are Dutra and Rockenbach Boardman (2006) mentioned characterized by foliage of the Brachyphyllum type, e.g., that ‘primitive forms of Araucariaceae’ were present B. mamillare definitely belongs to A. phillipsii (Harris since the Jurassic in the Antarctic Peninsula. Pollen 1979). This is also proved by attached male cones with in of Callialasporites type have been found in situ of situ pollen grains of the Araucariacites type (Kendall Masculostrobus Seward, 1911 in the Jurassic Beacon 1947) and Callialasporites type (van Konijnenburg-van Group in E Antarctica (Townrow 1967). There is also a Cittert 1971). Contrary to Stockey’s hypothesis on a substantial pollen record throughout the Jurassic in generalized araucarian type Ohsawa et al. (1995) Australia summarized in Kershaw and Wagstaff (2001). established a new extinct section of Araucaria for those The diverse record of wood in Gondwana is plants. Type of the section Yezonia Ohsawa, Nishida summarized in Bamford and Philippe (2001) suggesting and Nishida, 1995 is Araucaria vulgaris (Stopes and the occurrence of additional morpho-types distinctive Fujii, 1911) Ohsawa, Nishida and Nishida, 1995 from modern araucariaceous wood. consisting of the seed cone Araucaria nihongii Stockey, The Araucariaceae record in Eurasia (Fig. 9)is Nishida and Nishida, 1992 and the shoot Yezonia characterized by the occurrence of a distinct type of (Brachyphyllum) vulgare Stopes and Fujii, 1911 from Araucaria seed cone. Such cones originally placed in or the Late Cretaceous of Hokkaido, Japan (Ohsawa et al. near section Bunya of Araucaria (Stockey 1994) indicate 1995). a more ‘generalized’ araucarian type (Stockey 2002b) The Jurassic record of wood and pollen of Araucaria- with a mosaic of features of both Agathis and Araucaria. ceae is rather diverse (e.g., Philippe 1993; Dijkstra However, in gross morphology these cones resemble et al. 1999). It will be not mentioned in this paper. more Araucaria than Agathis. They show one-seeded cone scale complexes where seeds are embedded in tissue of the ovuliferous scale and usually a free tip of the ovuliferous scale called ligula. Araucaria sp. from the 6. Cretaceous ‘southern hemisphere’ record Morrison Formation, Utah, USA (Gee 2006); Araucaria sphaerocarpa Carruthers, 1866 from Middle Jurassic During the Cretaceous Araucariaceae have had Inferior Oolithe Formation in Bruton, Somerset, UK probably their widest distribution and their greatest (Stockey 1980a); Araucaria brownii Stockey, 1980 most diversity with records of all three extant genera and at likely from the Osmington Ooolite Series, Dorset, UK, least one extinct genus. The subsequent Palaeogene and Late Oxfordian, Late Jurassic (Stockey 1980b); Arau- Neogene record is characterized by the loss of taxa and carites phillipsii Carruthers, 1869 from the Yorkshire the loss of a wide range of areas all over the world flora, UK (Harris 1979); Araucaria moreauana Barale, (North America, Europe, Africa, Antarctica). The 1981 and several morpho-species from the Cretaceous of following data are compiled from modern literature to east Asia (see below) seem to belong to this type. supplement earlier published synopses on fossil Arau- Araucarites brodieri Carruthers, 1869 from the Middle cariaceae (Stockey 1994; Kershaw and Wagstaff 2001). Jurassic of Stonesfield, England (Cleal and Rees 2003), It focuses, first of all, on Gondwanan continents, Araucarites milleri Seward, 1911 from the Upper whereas the history of the family in the ‘‘northern Jurassic of Culgower, Scotland (van Konijnenburg-van hemisphere’’ is mentioned in the subsequent chapter. Cittert and van der Burgh 1989) and araucariaceous Due to the huge amount of published material this conifers from the Late Jurassic of Pe´ry-Reuchenette, compilation of references is far from being complete, but Swiss (van Konijnenburg-van Cittert and Meyer 1996) this is not the aim of the present paper. were not mentioned by Stockey (2002b) but seem to be The oldest substantiated Agathis and Wollemia fossils additional taxa that should be incorporated in the are from Australia and New Zealand (Fig. 10). The concept. A more detailed morphological and cladistic oldest known Agathis leaves (Agathis victoriensis Can- analysis is in need to define this extinct araucarian type trill, 1992) based on cuticle micromorphology come or types and to separate it or them from the genus from the late Early Cretaceous (Albian) of Victoria, Araucaria. The well-known and famous morpho-species Australia (Cantrill 1992). The oldest unequivocal A. mirabilis from the Jurassic of Patagonia (see above) Agathis seed cone dates from the Middle Eocene of SE may also belong to Stockey’s ‘generalized’ type (Stockey Australia (Carpentier and Pole 1995). ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 267

Fig. 10. Cretaceous record of putative Agathis fossils, putative Wollemia fossils, extinct genus Wairarapaia, and selected records of Araucaria seed cones, plotted in a simplified palaeogeographic map of the mid-Cretaceous in rectangular format (modified after Blakey 2005). (1) Agathis victoriensis, late Early Cretaceous, Australia (Cantrill 1992); (2) Wollemia (Dilwynites) pollen early Late Cretaceous (MacPhail et al. 1995; Chambers et al. 1998); (3) Araucarites wollemiaformis, late Early Cretaceous, Antarctica (Falcon- Lang and Cantrill 2001b); (4) Wairarapaia mildenhallii, mid-Cretaceous, New Zealand (Cantrill and Raine 2006); (5) Araucaria desmondii, section Perpendiculares, Late Cretaceous, New Zealand (Pole 1995); (6) diverse record of Araucariaceae pollen, Cretaceous, Australia (Kershaw and Wagstaff 2001); (7) Araucarioxylon sp., late Early Cretaceous, Antarctica (Falcon-Lang and Cantrill 2001a); (8) Araucarioxylon chapmanae and Araucariopitys antarcticus, Late Cretaceous, Antarctica (Poole and Cantrill 2001); (9) Araucaria antarctica, latest Late Cretaceous, Antarctica (Ce´sari et al. 2001); (10) Araucaria grandifolia, late Early Cretaceous, Argentina (del Fueyo and Archangelsky 2002), Alkastrobus peltatus, Araucariacites, Balmeiopsis, Cyclusphaera, late Early Cretaceous, Argentina (del Fueyo and Archangelsky 2005); (11) Araucaria sp., Araucariostrobus sp., late Early Cretaceous, Brazil (Kunzmann et al. 2004); (12) Araucariostrobus sp., upper Early Cretaceous, Columbia (van Waveren et al. 2002); (13) Dammaroxylon africanum, Late Cretaceous, South Africa (Schultze-Motel 1966); (14) Araucaria rogersii, Early Cretaceous, South Africa (Brown 1977); (15) Araucarioxylon dallonii, Early Cretaceous, Egypt (Dupe´ron-Lauoueneix and Lejal-Nicol 1981); (16) Agathoxylon lifiyii, Late Cretaceous, Egypt (Youssef et al. 2000); (17) Araucaria cutchensis, Early Cretaceous, India (Stockey 1994); (18) Araucarioxylon sp., latest Cretaceous, USA (Wheeler and Lehmann 2005); (19) Araucariopitys sp., Late Early Cretaceous, Canada (Harland et al. 2007); (20) for records in the European Cretaceous see Table 1; (21) Araucaria nipponensis, Araucaria vulgaris, Late Cretaceous, Japan (Ohsawa et al. 1995); (22) araucariaceous wood, Cretaceous, Thailand (Wang et al. 2006); (23) Araucarites pojarkovae, Latest Cretaceous to Danian, Russia (Krassilov 1976); for more detailed information see Sections 6 and 7.

Wollemia, that has distinctive pollen named Dilwy- So far, neither Agathis nor Wollemia have been nites (in the fossil record), dates back to the early Late demonstrated from South America, Africa and from Cretaceous (Turonian) in SE Australia (Fig. 10) and most parts of the northern hemisphere (except Agathis perhaps in New Zealand (MacPhail et al. 1995; in SE Asia). On the other hand, Araucaria seems to have Chambers et al. 1998). But, comparison of fossils with been relatively widely distributed since the Jurassic Wollemia has just started. Re-examination of some of (Fig. 10). This is due to the fact that palaeofloristic the fossil floras will probably reveal additional con- exchange between Gondwana (South America, Africa, tribution of fossil representatives to this genus in the Australia) and the Northern Hemisphere (North Amer- future. ica, Europe, Asia) was possible during the Jurassic, Cantrill and Raine (2006) described Wairarapaia perhaps until the Early Cretaceous. This might also mildenhallii from the Cretaceous (Albian-Cenomanian) imply a relatively late evolution of the genera Agathis of New Zealand (Fig. 10) as a new extinct araucarian and Wollemia during the latest Jurassic/earliest Cretac- cone related to Wollemia but showing distinct eous, when the successive breakup of Gondwana made seed morphology. This might be the first find of a migrations much more difficult. Kershaw and Wagstaff representative of the stem linage of the clade Agathis+ (2001) pointed out that initiation of continental rifting Wollemia (see Fig. 6). Synapomorphic feature is an in latest Jurassic and Early Cretaceous resulted in ovule or seed which is not fused to the cone scale the exclusion of India and Africa from subsequent complex. changes in Gondwanan vegetation. That may include ARTICLE IN PRESS 268 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 also immigration of Agathis and Wollemia. However, Patagonia, Argentina in mid-palaeolatitudes (del Fueyo the fossil record demonstrates that both Agathis and and Archangelsky 2002). Bunya is only known from the Wollemia have been restricted most likely to Australa- Jurassic (Stockey 1982), but Araucaria and Eutacta are sia, New Zealand and parts of Antarctica and did not present in the Cretaceous. Araucaria grandifolia Fer- reach other continents during the Early Cretaceous. An uglio from the Punta del Barco Formation, Patagonia, ecological and geographical analysis of extant Agathis Aptian, is confidently placed into section Araucaria species put forward the hypothesis that Agathis has that survived with two species in South America (del expanded its present range from two Gondwanan Fueyo and Archangelsky 2002). Additionally extinct centres: Australia and New Guinea (Whitmore and morphotypes of Araucaria may also occur. Notopehuen Page 1980). brevis, a plant with Brachyphyllum-like foliage, The widespread record of fossil Araucaria in Aus- araucarian cuticles and Araucariacites pollen in situ tralia, Tasmania and New Zealand was summarized has been established by del Fueyo (1991) from the recently by Hill (1995), Kershaw and Wagstaff (2001) Patagonian Cretaceous. Recently Kunzmann et al. and Dettmann and Clifford (2005). The proposal of a (2004) described B. obesum with typical araucarioid new extinct Araucaria section Perpendiculares Pole, 1995 cuticle micromorphology (Fig. 7) and seed cones cf. for fossil Araucaria leaves with stomatal orientation Araucaria sp. from the Late Aptian Crato Formation of predominantely transverse to the long leaf axis is Brazil, a southern hemisphere low-latitude Gondwanan noteworthy. This section contains actually only one flora. It can be argued that Yezonia-like morpho-types species: Araucaria desmondii Pole, 1995 from the early were found in mid-latitude northern hemisphere floras Late Cretaceous of New Zealand. (e.g., Yorkshire) during the Jurassic and the Cretaceous In Antarctica representatives of Araucariaceae are (Hokkaido) and in mid- to low-latitude southern hemi- common throughout the Cretaceous. Araucarioxylon sphere floras. from the mid-Aptian Cerro Negro Formation, Living- A remarkable diversity of Araucariaceae in Patagonia ston Island represents arborescent vegetation, which is also indicated by the occurrence of several pollen grew at 621S palaeolatitude (Falcon-Lang and Cantrill types in the Early Cretaceous strata. Araucariacites, 2001a). Balmeiopsis and Cyclusphaera are found inside micro- Cone scales putatively attributed to Wollemia are sporangia (del Fueyo and Archangelsky 2005), e.g., described as Araucarites wollemiaformis Cantrill and Cyclusphaera in Alkastrobus peltatus del Fueyo and Falcon-Lang, 2001 from the Late Albian of Alexander Archangelsky, 2005. Cones of Araucariostrobus from the Island. Within this palaeoflora at 751S palaeolatitude Lower Cretaceous of the Leiva region, Columbia, can several morpho-species of Araucaria (leaves, cone scales) not be assigned with certainty to the Araucariaceae (van co-occur (Falcon-Lang and Cantrill 2001b). Leaf Waveren et al. 2002). phenology analysis suggests that the araucarian and In Africa, fossil evidence of Araucariaceae is very podocarp conifers, which comprised more than 90% of rare. Schultze-Motel (1966) described wood as Dam- the canopy forming vegetation, were evergreen (Falcon- maroxylon africanum Schultze-Motel, 1966 from the Lang and Cantrill 2001a). Late Cretaceous (Late Senonian) of E Pondoland, South Different wood types (Araucarioxylon chapmanae Africa which clearly shows botanical affinities to both Poole and Cantrill, 2001; Araucariopitys antarcticus extant Araucaria and Agathis. Araucaria rogersii Brown, Poole and Cantrill, 2001) are studied by Poole and 1977 from the Early Cretaceous Kirkwood Formation Cantrill (2001) from the Late Cretaceous of Williams in the Cape Province, South Africa is regarded by Point Beds, Livingston Island indicating a remarkable Hernandez-Castillo and Stockey (2002) as putative fossil diversity in Araucariaceae. Wood and seed cones member of the Araucaria section Bunya. Araucarioxylon assigned to the new morpho-species Araucaria antarctica dallonii Boureau, 1948 from the Late Jurassic-Early Ce´sari et al., 2001 are described from the mid Cretaceous of Gebel Kamil, Egypt (Dupe´ron-Lauoue- Maastrichtian of Cape Lamb, Vega Island, Antarctica neix and Lejal-Nicol 1981) and Agathoxylon lifiyii (Ce´sari et al. 2001). It represents a component of a Late Youssef et al., 2000 from the Late Cretaceous of Kharga Cretaceous forest community growing under cold- Oasis, Egypt give evidence for a wide palaeogeographic temperate condition. range of fossil representatives of the family. The wood Polar forests dominated by Araucaria survived in record indicates also a common presence of Araucaria- Antarctica at least until mid-Eocene (Stephens et al. ceae in Africa throughout the Cretaceous period. In 2006). These fossil Araucaria remains from Seymour South Africa, Araucariaceae survived together with Island, Antarctic Peninsula have been identified as fossil other typical Gondwanan pollen taxa probably at least relatives to extant A. araucana of section Araucaria until the Neogene (Coetzee and Muller 1984). (Stephens et al. 2006). India, more exactly the Indian Tectonic Plate, was in In South America, three of the four extant sections of the Mesozoic part of Gondwana. During the Late Araucaria are represented in the fossil record of Cretaceous and Palaeogene it drifted very rapidly from ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 269 a southern hemisphere position northwards. In the Late above, A. nihongii was found attached to Brachyphyllum Cretaceous India reached an equatorial position with foliage shoot that resulted in the establishment of the tropical palaeoclimate. Several records of different extinct section Yezonia (Ohsawa et al. 1995). In SE Asia organs of Araucariaceae indicate a wide distribution in (northeast Thailand) the tropical palaeovegetation was the Cretaceous in India. Seed cones named Araucaria dominated by Araucariaceae in the Cretaceous indicated cutchensis (Feistmantel, 1879) Pant and Srivastava, 1968 by wood records (Wang et al. 2006). from the Early Cretaceous can probably included in the However, Araucariaceae were also common in high Araucaria section Eutacta (Stockey 1994). The occur- palaeolatitudes in the late Early Cretaceous to early rence of Araucarites in the Upper Gondwana Succession Late Cretaceous. The occurrence of Araucaria in a truly was recently summarized by Srivastava et al. (2004). polar vegetation (4721N palaeolatitude) is recorded by Araucaria indica Sukh-Dev and Zeba-Bano, 1976 from Spicer et al. (2002) from the uppermost Albian to the (Late Jurassic to) Early Cretaceous of Madhya- lowermost Cenomanian Grebenka flora, Krivorechevs- Pradesh is one of the best known ‘whole-plant’ kaya Formation in NE Russia. In the Yelisseev locality araucarian conifers from India. of the Grebenka flora Araucarites anadyrensis Kryshto- fovich, 1958 (foliage shoots) and male and female cones of Araucarites sp. have been found. They were growing under temperate (MAT 1371.8 1C) and humid climate 7. Cretaceous ‘northern hemisphere’ record (Spicer et al. 2002). In North America, Araucariopitys is abundant in Araucarian conifers disappeared from the palaeove- Aptian-Albian sediments in high palaeolatitudes getation of North America and Europe in the upper- (4601N; Harland et al. 2007). most Cretaceous. In northern Asia Araucarites The state of knowledge on European Araucariaceae pojarkovae Krassilov, 1976 from the Danian (Early (Table 1) was recently summarized by Kunzmann Palaeocene) of Amur Land is the youngest record (2007). It is shown that Araucariaceae are rare elements (Krassilov 1976, 1978), while in SE Asia (Malay within the European Late Cretaceous vegetation as Peninsula) Agathis survived until today. Generally proven throughout the Cretaceous system. Araucaria Araucariaceae were more widespread in SE Asia carolae Kunzmann, 2007, a permineralized fragmentary (Cambodge, Laos, Vietnam) until the Pleistocene seed cone from the Early Cretaceous (Aptian/Albian) of (Vozenin-Serra and Prive´-Gill 1991). Last occurrence Brilon-Nehden, Nordrhein-Westfalen, Germany, shows in Europe is published by van der Ham (2004) who morphological features typical for northern hemisphere described a seed-cone scale complex of an Araucaria sp. Araucaria in the Jurassic and Cretaceous (Kunzmann from the Maastrichtian type area in the Netherlands. 2007; Fig. 11). Thus this morpho-species might belong Additionally possible Araucariaceae foliage is reported to an Araucaria type showing affiliations to both by van der Ham et al. (2003) from the same locality. The section Eutacta and Bunya or to Stockey’s ‘generalized’ youngest evidence of Araucariaceae in North America is araucarian type. provided by wood from the Maastrichtian Javelina Araucaria fricii Velenovsky´in Bayer, 1893 emend. Formation exposed in the Big Bend National Park, Kunzmann (2007) is described from the Early to Middle Texas, USA (Wheeler and Lehmann 2005). Coniacian Brˇezno Formation in North Bohemia, Czech As mentioned above, neither Agathis nor Wollemia Republic (Bayer 1893; Fig. 12) and from the Late have been demonstrated to occur in the fossil record of Santonian Aachen Formation in Hauset, Belgium North America, Europe and N Asia. However, the (Kunzmann 2007; Fig. 13). This seed cone morpho- existence of extinct genera might be concluded from species shows similarities to extant species of Araucaria several distinct ‘organ-taxa’ like Dammarophyllum (foli- section Eutacta. In both localities araucarioid foliage is age) and Balmeiopsis (pollen). associated in the taphocoenoses (Kunzmann 2007). An excellent compilation of fossil Araucariaceae was Additionally, araucariaceous wood is described as recently given by Dijkstra et al. (1999) containing Dammaroxylon aachenensis Meijer, 2000 from the numerous records from the Cretaceous of Asia. Herein Aachen Formation. only a few important records are mentioned. Perfectly The systematic position of several morpho-types of permineralized seed cones have been found in the Late isolated cone scales (e.g., Dammara borealis Heer, 1882; Cretaceous of Hokkaido, Japan (Stockey et al. 1992, Aachenia debeyi Knobloch, 1972) is still debated. The 1994). Araucaria nipponensis Stockey, Nishida and majority probably cannot be assigned to Araucariaceae. Nishida, 1994 and A. nihongii previously assigned to From the morphological and cuticular point of view, section Bunya (Stockey 1994; Hernandez-Castillo and such scales might be Cretaceous representatives of the Stockey 2002) support the concept of a ‘generalized’ Doliostrobaceae (Kunzmann 1999; Bosma et al. 2006). araucarian type in the Mesozoic of the northern One of the most interesting questions concerning the hemisphere suggested by Stockey (2002b). As mentioned family’s history is that of the disappearance in latest ARTICLE IN PRESS 270 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Table 1. Fossil record of Araucariaceae in the European Cretaceous. Modified from Kunzmann (2007)

Stratigraphy Localities Taxa References

Palaeogene Late Cretaceous Maastrichtian Maastricht Formation Araucaria sp. van der Ham (2004) Campanian Santonian Aachen Formation (Belgium, Germany) Araucaria fricii Kunzmann (2007) Araucaria crassifolia Kra¨usel (1922) Dammaroxylon Meijer (2000) aachenense Dadoxylon cf. Gottwald (2000) subherzynicum ?Aachenia debeyi Knobloch (1972), Bosma et al. (2006) Heidelberg Formation (Germany) Dadoxylon subhercynicum Schultze-Motel (1962) Coniacian Klikov Formation, Senonian (Czech ?’’Dammara’’ borealis Ne˘mejc and Kvacˇek (1975) Republik) Brˇezno Formation (Czech Republic) Araucaria fricii Velenovsky´in Bayer (1893) Araucaria brachyphylla Bayer (1893) Turonian Cenomanian Peruc-Korycany Formation (Czech Dammarites albens Kvacˇek (1998) Republic) ?Dammarophyllum Kvacˇek (2003) striatum

Fouras (France) Agathoxylon sp. Ne´raudeau et al. (2003)

Early Cretaceous Albian La´batlan Formation (Hungary) Agathoxylon pannonicum Barale et al. (2002) Archingeay (France) Agathoxylon sp. Perrichot (2004)

Aptian Brilon-Nehden (Germany) Araucaria carolae Kunzmann (2007) Araucaria sp. Kampmann (1983) Araucariaceae-plantula Wilde and Goth (1987) Several localities in France and Italy Several taxa (not revised) B. Gomez (pers. comm.) Barremian Buarcos, Arunitos de Carrascal (Portugal) Araucariacites australis Groot and Groot (1962) Hauterivian Valanginian Sierra du Montsec (Spain) Araucarites pedreranus Barale (1989) Dammarites coriacea Barale (1992) Berriasian Aquitaine Basin (France) Agathoxylon sp. El Albani et al. (2004) Jurassic

Cretaceous from the ‘northern hemisphere’. In mid- predestined to become extinct whenever remarkable Cretaceous Araucariaceae were part of the Araucaria- environmental changes may take place. Elatides-Classopollis forest of the mid-latitudes in North The disappearance coincides with two major events in America and Eurasia (Krassilov 1978). In the Late earth history. At first, major changes in forest composi- Cretaceous Araucariaceae can be considered as relics in tion in the European-North American Normapolles the palaeovegetation like Lindleycladus and Nilssonia floristic province may have contributed to the decrease Brongniart, 1825. In Europe, Araucariaceae were in araucarians. The Normapolles complex constitutes an accessory elements of the lowland vegetation probably important and diverse element of Late Cretaceous floras not or never prominent in the Cretaceous landscape in the northern hemisphere, especially in the Atlantic (Kunzmann 2007). In this context one has to expect a North America, Europe and western Asia, a region gradual decline of taxa and individuals in the Late called Normapolles floristic realm or province in mid Cretaceous. A relict status means that they were and Late Cretaceous (Mai 1995). Although it is difficult ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 271

Fig. 11. Araucaria carolae Kunzmann, 2007, holotype, Calcit quarry Henke, SW’ Nehden, Brilon-Nehden, Sauerland, Nordrhein- Westfalen, Germany, Aptian/Albian, Collection of the Ruhrlandmuseum Essen, Germany, RE 551.763.120 A0349/1–5 (from Kunzmann 2007). (A) Fragmentary seed cone (arrow showing fracture which supplies internal view in B); (B) horizontal cross section showing gross morphology of cone scales and seeds.

morphology suggests wind pollination of Normapolles plants. This evolution in Late Cretaceous vegetation was caused by variation or changes in palaeoclimate. There was a dramatic decrease of Normapolles elements in vegetation in the latest Cretaceous (Mai 1995). So, Araucariaceae as typical wind pollinators were probably also not able to survive under changed conditions. Second, most recent populations might have been killed by dramatic short-term environmental changes following the meteorite impact event at the K-P boundary. However, there might be a multicausal explanation to understand this regional extinction phenomenon which is far from being settled.

8. Summary

Today, Araucariaceae are represented by only three genera (Agathis, Araucaria, Wollemia) with 41 species that are almost confined to the southern hemisphere. Fig. 12. Araucaria fricii Velenovsky´in Bayer, 1893, seed-cone They occupy a typical Gondwanan relict area. Mor- scale complex, holotype Bayer (1893): Fig. 1,Brˇezno, province phological and molecular analyses prove that Wollemia Severocˇesky´Kraj, Czech Republic, Early-Middle Coniacian, is sister to Agathis, and Araucaria is sister to the clade Late Cretaceous, Palaeontological collection of the National Agathis+Wollemia. The most recent common ancestor Museum Prague, Czech Republic, NM F 1898 (from of Agathis and Wollemia is at least 110 Ma old Kunzmann 2007). (A) Cone scale complex from adaxial, seed deduced from the oldest Agathis and Wollemia fossils removed (scale bar: 10 mm); (B) fragment of the seed (cast) which are Aptian (Early Cretaceous) in age. removed from A (scale bar: 2 mm). In the geologic past Araucariaceae were more wide- spread as indicated by the generally patchy and sparsely to assess systematic affinities to the Normapolles fossil record. Araucariaceae have had a nearly world- elements, for many relationships to extinct Fagales wide distribution in the Mesozoic but have been and Juglandales were proposed (Friis et al. 2006). Pollen restricted since the Palaeogene (Middle Palaeocene) to ARTICLE IN PRESS 272 L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277

Fig. 13. Araucaria fricii Velenovsky´in Bayer, 1893, quarry Bingeberg Flo¨g near Hauset, province Verviers, Belgium, Aachen Formation, Late Santonian, Late Cretaceous, private collection H. Knoll, Alsdorf, Germany, No. 415 (from Kunzmann 2007). (A) fragmentary seed cone in apical-lateral view; (B) internal view showing seeds (grey) embedded in tissue of the ovuliferous scales (white) (scale bar: 10 mm).

the southern hemisphere with an extension into the record is required for a better understanding of the northern hemisphere in SE Asia. Reasons for disap- history of the family. pearance of representatives of the family in the latest Cretaceous in North America and Europe and in the Early Palaeocene in northern Asia are probably climatic Acknowledgements changes and angiosperms as general competitors in the vegetation. In the case of Europe and the Atlantic part Thanks go to Uwe Fritz (Dresden) inviting me for a of North America changes in forest composition in the presentation at the 48th Phylogenetic Symposium in Normapolles province should be taken in consideration. Dresden. I am indebted to Susanne Renner (Munich) Finally, there may be a certain influence by the meteorite who critically discussed molecular methods in recon- impact at the K-P boundary. structing phylogenetic relationships in Araucariaceae Araucariaceae probably evolved in the Triassic from with me. As a result she proposed to figure an voltzialean conifers. The centre of origin is unknown, unpublished cladogram in this paper (Fig. 6). I am but a Gondwanan origin is suggested by earliest grateful to an anonymous reviewer and Johanna H. A. fossil records. The family expanded and diversified in van Konijnenburg-van Cittert (Leiden) for constructive both hemispheres in the Late Triassic and Jurassic. comments on the manuscript and additional advice to The existence of the Pangaea super-continent had a literature. Thanks to Jirˇi Kvacˇek (Prague), Bernard positive effect on migration processes. The fossil record Gomez (Rennes), Raymond van der Ham (Leiden) and yielded specimens of extinct genera which provide Dieter Hans Mai (Berlin) for helpful discussions. evidence of a significantly higher diversity in the past. This diversity is indicated by extinct types of seed cones, pollen, wood and foliage. The genus Araucaria References tends back to the Middle Jurassic and its area extended in the Jurassic and Cretaceous into the Northern Archangelsky, S., 1979. Balmeiopsis, nuevo nombre gene´rico hemisphere. In contrast, those specimens from the palinomorfo Inaperturopollenites limbatus Balme. Ame- Jurassic and the Cretaceous of the northern hemisphere ghiniana 14, 122–126. assigned to Araucaria may be also interpreted as Archangelsky, S., 1994. Comparative ultrastructure of three morpho-species of a ‘generalized’ araucarian type. Thus, early Cretaceous gymnosperm pollen grains: Araucaria- they may represent the stem lineage of the family. The cites, Balmeiopsis and Callialasporites. Rev. Palaeobot. species of the genera Agathis and Wollemia evolved in Palynol. 83, 185–198. Bamford, M.K., Philippe, M., 2001. Jurassic – Early Cretac- the Early Cretaceous in southern Gondwana (Australia, eous Gondwanan homoxylous woods: a nomenclatural Antarctica, New Zealand). These genera were probably revision of the genera with taxonomic notes. Rev. confined to Gondwanan continents. Compilation of Palaeobot. Palynol. 113, 287–297. literature data shows a couple of problems still Barale, G., 1981. La paleoflore Jurassique du Jura franc¸ais: unresolved. An extended phylogenetic analysis of all Etude systematique, aspects stratigraphiques et paleoeco- extant species combined with the data of the fossil logiques. Doc. Lab. Geol. Lyon 81, 1–467. ARTICLE IN PRESS L. Kunzmann / Zoologischer Anzeiger 246 (2007) 257–277 273

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