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Seed-cone scales from the upper Maastrichtian document the last occurrence inEurope of the Southern Hemisphere conifer family Araucariaceae

Raymond W.J.M. van der Ham a,⁎, John W.M. Jagt b,Sjir Renkens c, Johanna H.A. van Konijnenburg-van Cittert d

a Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, P.O. Box 9514, NL-2300 RA Leiden, The Netherlandsb Natuurhistorisch Museum Maastricht, De Bosquetplein 6, NL-6211 KJ Maastricht, The Netherlandsc Nieuwe Tijningen 33, NL-5301 DA Zaltbommel, The Netherlandsd Netherlands Centre for Biodiversity Naturalis, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands

a b s t r a c ta r t i c l e i n f o

Article history:Received 7 October 2009Received in revised form 9 February 2010Accepted 10 March 2010Available online 15 March 2010

Keywords:AraucariaClimate changeConifer cone scaleFossilLast appearance datumMaastrichtian

Stratigraphically well-documented seed-cone scales belonging to the conifer genus Araucaria have recentlybeen collected from marine upper Maastrichtian (uppermost Cretaceous) limestones in the type area of theMaastrichtian Stage (NE Belgium, SE Netherlands). These fossils document the youngest known occurrencesof the Monkey Puzzle family (Araucariaceae) in Europe, extending the last appearance datum (LAD) forEurope ‘upwards’ in time for c. 18 million years. The cone scales can barely be distinguished from those of theextant Araucaria heterophylla, today confined to Australia. Together with an equally close similarity to anEarly Jurassic scale from North America, these finds illustrate the great antiquity and constancy of seed-conemorphology within Araucaria section Eutacta. Climate change and competition with angiosperms, ratherthan the impact of a large extraterrestrial body (Cretaceous/Paleocene boundary event), led to the demise ofAraucaria in the Maastrichtian type area.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

The earliest records of the classic Southern Hemisphere coniferfamily Araucariaceae date back to the Late Triassic, more than200 million years (Ma) ago, as epitomised by the Petrified Forest,Arizona, USA(AxsmithandAsh, 2006).Nowadays, this family comprisesthree surviving genera (Farjon, 2001), namely Agathis (21 species, e.g.A.australis, Kauri), Araucaria (19 species, e.g. A. araucana, Monkey Puzzle)and a single species of Wollemia (W. nobilis, Wollemi Pine), which wasdiscovered in an inaccessible gorge near Sydney, Australia as recent as1994 (Jones et al., 1995). The prickly Monkey Puzzle from temperateSouth America is a well-known garden plant in Europe. Phylogeneti-cally, Araucaria is placed as sister to Agathis + Wollemia on bothmorphological and molecular evidence (Kunzmann, 2007).

The extensive fossil record of the Araucariaceae shows that theJurassic (c. 200–145 Ma) and Cretaceous (c. 145–65 Ma) were periodsof high diversity and near-cosmopolitan distribution (Kunzmann,2007). The trees were probably prominent elements in the landscape,especially in southern continents (Gondwana). From the Late Creta-ceous onwards the family gradually declined, in number of species as

well as geographically, retreating from the Northern Hemisphere toseveral relict areas in the Southern Hemisphere. The discovery ofaraucariaceous seed-cone scales in strata of Late Maastrichtian age inBelgium and The Netherlands now enables an unambiguous statementabout the last European representatives of the Araucariaceae and theiraffinities with extant members of the family.

2. Material, localities and stratigraphy

Three stratigraphically well-documented seed-cone scales havebeen collected in recent years (2002–2009), two of them by J.W.M.Jagt at the ENCI-HeidelbergCement Group quarry near Maastricht(southern Limburg, The Netherlands), the other by S. Renkens at theMarnebel quarry near Eben-Emael (Liège, Belgium), about four kilo-metres south of the ENCI quarry. Both localities are within theMaastrichtian type area. The stratigraphically oldest specimen(NHMM JJ 12463) originates from the basal part (lower 0.3 m) of theGronsveld Member, the two younger ones (NHMM JJ 14282, SR 523)from the upper part (upper 3 m) of the Emael Member (i.e., above theLava horizon). Both units belong to the fully marine MaastrichtFormation, which is of latest Maastrichtian (Late Cretaceous) age(Fig. 1); detailed descriptions and lithological logs of these units werepublished by Jagt (1999) and Felder and Bosch (2000). Fragmentarytests of two echinoid species (Hemiaster prunella, Hemipneustesstriatoradiatus), an ostreid bivalve (‘Acutostrea’ uncinella), a serpulid

Palaeogeography, Palaeoclimatology, Palaeoecology 291 (2010) 469–473

⁎ Corresponding author. Tel.: +31 71 5273593; fax: +31 71 5273511.E-mail addresses: ham@nhn.leidenuniv.nl (R.W.J.M. van der Ham),

John.Jagt@maastricht.nl (J.W.M. Jagt), sjir.renkens.geo@xs4all.nl (S. Renkens),Konijnenburg@naturalis.nnm.nl (J.H.A. van Konijnenburg-van Cittert).

0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved.doi:10.1016/j.palaeo.2010.03.017

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Fig. 1. Stratigraphy of Upper Cretaceous deposits in the Maastrichtian type area, showing the provenance of the Araucaria seed-cone scales.

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(Pyrgopolon mosae), seagrass (Thalassocharis bosquetii) and severalunidentifiable plant remains were found associated with the scales inthe medium-grained biocalcarenitic matrix.

The following abbreviations are used to indicate the repositoriesof the specimens: NHMM: Natuurhistorisch Museum Maastricht(Maastricht, The Netherlands), SR: private collection of Sjir Renkens(Zaltbommel, The Netherlands).

3. Description, interpretation and taphonomy

The seed-cone scales are wedge shaped and 20 to 28 mm long(i.e., from base to top). They have two lateral wings and an irregularshallowdepression is evidentnear thedistal edge. Each scale possesses acentral bulging body (seed),which is elongate-obovate, 16–20 mmlongand 6–8 mm wide (Fig. 2a, b). These fossils can be unambiguouslydefined as scales of Araucaria seed cones, the bulging body in the centreof each scale representing a seed extensively fused to the scale.

Near-mature seed cones of Araucariaceae consist of scales tightlyarranged on a central axis. The scales detach from the axis at maturity.The upper (adaxial) surface of a scale bears a single seed,which remainsfused to the scale in Araucaria but is shed from the scale in Agathis andWollemia. The bulging shape of the seeds indicates that they wereresistant to compression, probably due to the presence of a thick rigidseed coat. The free distal extension (ligule) of the seed-bearing part,which is more or less distinct in fresh material (Figs. 3 and 4), is notpreserved in the fossils. The irregular shallow depressions observed inthe distal scale margins are interpreted as the imprints of the thickerdistal parts of the scales. The wings were thin, as suggested by theirrelatively light brown colour, compared with the darker brown centraland distal parts (compare Fig. 2a with Fig. 3c). In near-mature seedcones of Araucaria the thin wings of the scales are situated between theclosely packed seed-bearing parts of adjacent scales. After detachmentof the scales from the cone axis, the wings aid and may account for theoccurrence of the fossils in the fully marine deposits of the Maastricht

Formation. The fine preservation of the thin wings indicates thattransport was gentle and/or that the parent trees grew close to the sitesof deposition.

4. Nearest relatives and ecology

Seeds of extant species of Araucaria are 15–60 mm long and 6–32mm wide: those of the section Araucaria (2 species): 30–50×10–20mm, section Bunya (1 species): 40–60×23–32 mm, section Eutacta(15 species): 15–35×6–14 mm, and section Intermedia (1 species): 25–28mmlong.Morphologically, the fossil scales are similar to the scales ofA. heterophyllaof the section Eutacta (Fig. 3c), being only slightly smaller(seeds 16–20×6–8 vs. 22–30×8–12 mm). The seeds of the other threesections are larger and/or the scales contrast in morphology: wingsvestigial in the section Araucaria (Fig. 3a), thick and rigid in Bunya(Fig. 3b) and relatively large in Intermedia (Fig. 3d). Living species of thesection Eutacta are more or less restricted to tropical montanerainforests. Applying the Nearest Living Relative approach (NLR; Tayloret al., 2009), this indicates a similar environment for the MaastrichtianAraucariaceae in Europe. The occurrence in the lower part of theMaastricht Formation of twigs of other conifers and diverse angiospermleaves suggests that they did not grow in Araucaria forests but wereelements of a mixed conifer/angiosperm forest type. In contrast to thebulky seeds found in the sections Araucaria and Bunya, the fossil seedswereprobably not aprofitable food source formost animals, the seedsofspecies of Eutacta being relatively lightweight and small and hencebetter adapted to dispersal by wind. In view of the size of the fossilscales, the parent conesmust havemeasured between 50 and 60 mm inwidth.

5. Palaeobiogeography and phylogeny

Classifying the seed-cone scales within the section Eutactaconfirms that the present Southern Hemisphere distribution of this

Fig. 2. Fossil Araucaria seed-cone scales from the Maastricht Formation (late Maastrichtian) in the Maastrichtian type area. (a) Specimen NHMM JJ 12463 from the basal part of theGronsveld Member, showing scale base (below), ‘right’wing and fragment of ‘left’wing, and the elongate–obovate seed in the centre. (b) Specimen SR 523 from de Emael Member,above the Lava horizon, showing scale base (below), large fragments of both wings, and the elongate–obovate seed in the centre.

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section is relictual. Connections with the Northern Hemisphere goback to the Jurassic, in which the section Eutacta was alreadyrepresented in Europe (Harris, 1979) and North America (Axsmithet al., 2008). The latter authors also compared a seed-cone scale fromthe Lower Jurassic (first appearance datum of the section Eutacta)with scales of extant Araucaria heterophylla. The close resemblance ofthe Early Jurassic and Maastrichtian material to scales of this speciesimplies that the seed cones themselves were also probably alike(Fig. 4). As seed-cone morphology changed little if at all from theJurassic onwards, we can legitimately describe the cones of modernspecies of Araucaria section Eutacta as ‘living fossils’.

6. Last of the European Araucariaceae

Araucaria was a rare element in the Late Cretaceous flora ofEurope, while the younger and more derived genera Agathis andWollemia are totally unknown from Europe. Fossil Araucaria pre-dating our Maastrichtian material has been recorded from Santonian(85.8–83.5 Ma; Gradstein et al., 2004) deposits in the east of theMaastrichtian type area and adjoining German territory (Kunzmann,2007). The youngest specimen in our material is from the uppermostthree metres of the Emael Member (Maastricht Formation), above theLava horizon dated to c. 65.75 Ma (Vonhof and Smit, 1996). Thismeans that the last appearance datum (LAD) of Araucaria in Europecan be confidently extended ‘upwards’ in time by c. 18 million years.

Our scales document the last known indigenous occurrences of theAraucariaceae in Europe.

The youngest records of the Araucariaceae in North America arebased on Late Cretaceous to Paleocene woods from Texas (Kunzmann,2007). However, there is no reliable way of determining whether theseisolated pieces represent araucariaceous species or the extinct familyCheirolepidiaceae (Wheeler and Lehman, 2005). The last record fornorthern Asia is based on material from Danian (lower Paleocene)deposits in the Amur region, Far East Russia, described byKrassilov (1976,1978) as Araucarites pojarkovae. However, part of that material hassubsequently been reassigned to the angiosperm family Cercidiphyllaceae(Golovneva, 2006;KrassilovandKodrul, 2006),while theseed-cone scalesdiffer from those of Araucaria (scale longitudinally ribbed, seed 5mmlong) and probably belong to the family Doliostrobaceae instead (Kvaček,2002; Z. Kvaček, Personel communication, 2009). Thus, it appears that theLate Maastrichtian scales from Belgium and The Netherlands may evenrepresent the youngest araucarian records for the greater part of theNorthern Hemisphere. The genus Agathis survives in Southeast Asia.

The disappearance of Araucaria from Europe pre-dates by c.250,000 years the Cretaceous/Paleocene (K/P) boundary event, whichequates with the presumed impact of a large extraterrestrial body(Chicxulub crater, Mexico; Nichols and Johnson, 2008). The Europeanaraucarians may have fallen victim to the same perturbations thateventually led to the extinction of gymnosperm seed plants such asthe Cheirolepidiaceae (Van der Ham et al., 2003; Van der Ham and

Fig. 3. Araucaria seed-cone scales of extant species. (a) A. araucana (Monkey Puzzle; section Araucaria), cultivated, The Netherlands. (b), A. bidwillii (Bunya-bunya Pine; sectionBunya), cultivated, Portugal. (c), A. heterophylla (Norfolk Island Pine; section Eutacta), cultivated, Corfu, Greece. (d), A. hunsteinii (section Intermedia), Brass 32322 (NetherlandsCentre for Biodiversity Naturalis, section NHN), New Guinea. Adaxial surfaces of dry material; white spot indicates ligule.

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Dortangs, 2005) and the Bennettitales, and of non-avian dinosaurs.Climate change and competition with angiosperms, which led tomajor shifts in forest composition (Kunzmann, 2007), may have beenimportant factors in this process. Cooling during the latest Maas-trichtian in the type area of the stage is clearly indicated by themarkedly decreased spore diversity and the disappearance ofCheirolepidiaceae pollen (Classopollis–Classoidites) in the upperpart of the Maastricht Formation, from about the Lava horizon up-wards (Herngreen et al., 1998; Van der Ham et al., 2003).

7. Conclusions

Seed-cone scales from the upper Maastrichtian in the Maastrich-tian type area (Belgium and The Netherlands) document the lastknown, indigenous occurrences of Araucaria (and hence of the familyAraucariaceae) in Europe. In view of the close similarity to the seed-cone scales of extant Araucaria heterophylla, they are identified asbelonging to the Southern Hemisphere Araucaria section Eutacta.Together with the equally strong resemblance to Early Jurassicmaterial from North America, this demonstrates the great antiquityand constancy of seed-cone scale morphology within this section.Consequently, the seed cones themselves were probably also quitesimilar. Deteriorating climatic conditions and competition withangiosperms may have been responsible for the disappearance ofAraucaria in the type area during the latest Maastrichtian.

Acknowledgements

We wish to thank Ben Kieft (Netherlands Centre for BiodiversityNaturalis, section NHN) for producing the illustrations, Zlatko Kvaček(Charles University, Prague) for valuable information on the identity ofAraucaria material from Russia, Erik Smets (Netherlands Centre forBiodiversity Naturalis, section NHN) and Elisabeth Wheeler (NorthCarolina State University, Raleigh) for comments on an earliertypescript, and Richard Bateman (Royal Botanic Gardens, Kew) and ananonymous reviewer for their very useful comments on the earliersubmitted version.

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Fig. 4. Seed cone and twig of Araucaria heterophylla (Norfolk Island Pine; sectionEutacta), cultivated, Kos, Greece. This cone shows how the fossil cones from theMaastrichtian probably appeared in the living state. Note the ligule (above and behindspine) on top of each cone scale. The horizontal cone diameter is 76 mm.

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