Taphonomy and Palaeoecology of Mid-Cretaceous Amber-Preserved Microorganisms from Southwestern France

Taphonomy and palaeoecology of mid-Cretaceous amber-preserved microorganisms from southwestern France

Vincent GIRARD Université Rennes I, UMR CNRS 6118 Géosciences, campus de Beaulieu bât. 15, 263 avenue du Général Leclerc, F-35042 Rennes cedex (France) [email protected]

Alexander R. SCHMIDT Stefﬁ STRUWE Courant Research Centre Geobiology, Georg-August-Universität, GöttingenGoldschmidtstraße 3, D-37077Göttingen (Germany) and Museum für Naturkunde der Humboldt-Universität zu Berlin, Invalidenstrasse 43, D-10115 Berlin (Germany)

Vincent PERRICHOT Paleontological Institute, University of Kansas, Lindley Hall, 1475 Jayhawk blvd, Lawrence, KS 66045 (USA) Gérard BRETON Didier NÉRAUDEAU Université Rennes I, UMR CNRS 6118 Géosciences, campus de Beaulieu bât. 15, 263 avenue du Général Leclerc, F-35042 Rennes cedex (France)

Girard V., Schmidt A. R., Struwe S., Perrichot V., Breton G. & Néraudeau D. 2009. — Taphonomy and palaeoecology of mid-Cretaceous amber-preserved microorganisms from southwestern France. Geodiversitas 31 (1) : 153-162.

ABSTRACT Th e investigation of microorganisms preserved in amber from Charente- Maritime (southwestern France) provides new insights into the mid-Cretaceous amber forest ecology. Amber from the localities of Archingeay-Les Nouillers and Cadeuil is unique due to the plethora of microinclusions and macroinclu- sions as well as the preservation of litter organisms. Soil microorganisms such as actinomycetes, sheathed prokaryotes, carnivorous fungi (Ascomycota), algae, KEY WORDS Palaeoecology, testate amoebae and nematodes indicate that the resin solidifi ed in terrestrial or taphonomy, limnetic-terrestrial microhabitats on the forest fl oor. Furthermore, arboreal and amber forests, even marine microorganisms are preserved in the amber. Th is micro-assemblage microorganisms, Cretaceous, suggests that the amber forest was located close to the sea shore or was at least France. temporarily under marine infl uence.

GEODIVERSITAS • 2009 • 31 (1) © Publications Scientiﬁ ques du Muséum national d’Histoire naturelle, Paris. www.geodiversitas.com 153 Girard V. et al.

RÉSUMÉ Taphonomie et paléoécologie des microorganismes préservés dans l’ambre médio- crétacé du sud-ouest de la France. L’investigation des micro-organismes préservés dans l’ambre de Charente- Maritime (sud-ouest de la France) fournit de nouveaux indices sur les écosystèmes fores- tiers à ambre médio-crétacés. L’ambre des localités d’Archingeay-Les Nouillers et de Cadeuil est unique par l’abondance de micro- et macro-inclusions ainsi que par la préservation d’organismes de litière. Des micro-organismes du sol tels que des actinomycètes, des procaryotes gainés, des champignons carnivores (ascomycètes), des algues, des amibes testées et des nématodes, indiquent que la MOTS CLÉS Paléoécologie, résine s’est solidiﬁ ée dans des micro-habitats terrestres ou limniques-terrestres taphonomie, au niveau du sol de forêt. En outre, des micro-organismes arboricoles et même forêts à ambre, marins sont également préservés dans cet ambre. Ce micro-assemblage suggère micro-organismes, Crétacé, que la forêt à ambre était située à proximité de la mer ou était au moins tempo- France. rairement sous inﬂ uence marine.

INTRODUCTION Th ough extensive studies have been launched in the last years on this arthropod fauna, only few Amber localities of southwestern France are known works have been attempted on the microfossils for a couple of hundred years (Fleuriau de Bellevue preserved in this amber. Galippe (1920) men- 1817; for more details, see Néraudeau et al. 2009 this tioned the presence of microbes in amber from volume). However, before its re-discovery in 1999 Enet Island (Charente-Maritime) and Berland by Didier Néraudeau and his team (Néraudeau et al. (Charente). He noticed that some of the bac- 2002, 2008, 2009 this volume; Perrichot 2005), teria he found were able to develop on growth amber from these localities has never been exten- medium in the laboratory. This observation sively investigated. Nowadays, the amber deposits of suggests that they were not fossil bacteria but the Charentes region are known for the plethora of merely contaminants of the amber. More recently arthropods they contain (Perrichot 2005). In addi- Schlüter (1978) investigated amber from Enet and tion, studies on the palaeobotany and depositional Aix islands but he failed to fi nd any macro- or environment provided many palaeoecological de- microinclusions. Breton & Tostain (2005) and tails (Néraudeau et al. 2002, 2008; Perrichot 2005; Breton (2007) mentioned that some sheathed Vullo 2007). Two particular localities, Archingeay- prokaryotes found in Charentes amber look very Les Nouillers and Cadeuil, provide new insights similar to those described as Palaeo colteronema into the mid-Cretaceous terrestrial environments cenomanensis Breton & Tostain, 2005 from the from Western Europe in terms of arthropod fauna, Cenomanian amber of Écommoy (northwestern vertebrate fauna and fl ora (Perrichot 2005; Vullo France). Finally, Néraudeau et al. (2008) men- 2007). Up to now, the large amount of amber col- tioned some cyanobacteria, bacteria and fl agellate lected in quarries of Archingeay-Les Nouillers and algae preserved in Cadeuil amber but without Cadeuil allowed the discovery of more than 1000 any detailed description. fossil arthropods including mainly dipterans and Here we report palaeoecological implications hymenopterans but also neuropterans, orthopterans, based on the investigation of microinclusions of coleopterans, arachnids, and crustaceans (Perrichot several highly fossiliferous pieces from Archingeay 2004, 2005). and Cadeuil which help to better understand the

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taphonomy and palaeoecology of microorganisms Th e amber pieces were investigated using high- in their forested environments 100 million years magnifi cation transmitted light microscopy (Leica ago. DMLP, Nikon Optiphot). Th e amber pieces investigated are deposited in the Muséum national d’Histoire naturelle, Paris MATERIAL AND METHODS and in the collection of the laboratory Géosciences Rennes (University Rennes I) (see fi gure legends for The amber containing the microcoenoses de- accession numbers). scribed here was collected from Late Albian layers of Archingeay-Les Nouillers and Cadeuil quarries. In both localities amber layers (from the litho- OBSERVED MICROCOENOSES logical subunit A1; Néraudeau et al. 2002, 2008) are well developed within lignitic clay lenses that Investigations of Archingeay-Les Nouillers and range from 0.1 to 1 m in thickness. Th is amber Cadeuil ambers revealed that microorganisms of and the associated fossil wood were deposited in at least three diff erent habitats are preserved, since a coastal marine area, as indicated by the presence litter-dwelling, arboreal and marine organisms occur, of oysters, teredinid bivalve holes in the wood, and sometimes together in a single piece of amber. marine foraminifera in the lignitic clay (Néraudeau et al. 2002; Perrichot 2005). More than 100 kg of LITTER-DWELLING AND SOIL-LIVING amber were collected in these quarries so far. Th e MICROORGANISMS present study describes the results obtained from Most microorganisms found in this amber are lit- highly fossiliferous pieces of two diff erent kinds ter- or soil-living taxa. Sheathed prokaryotes are of amber. One has been described as litter amber the most abundant microinclusions. Most sheathed by Perrichot (2004). It represents stratifi ed amber fi laments are 6-10 μm in diameter (Fig. 1F) and pieces with dark layers at the bottom becoming are morphologically similar to the cyanobacterium more and more translucent from one side to the Palaeocolteronema cenomanensis and to the sheathed other. Th ese amber pieces are exceptionally rich in bacterium Leptotrichites resinatus Schmidt & Schäfer, arthropods. It is suggested that the resin fl owed di- 2005. Th ese fi liform inclusions sometimes form a rectly to the forest fl oor since many arthro pods are 0.2 to 1.5 cm thick peripheral cortex in the amber litter-living inhabitants. Th e second kind is mainly pieces. Measurements of phycocyanin allow to prove composed of fl attened pieces of dark red amber that they correspond to P. cenomanensis (Girard et characterized by a greyish to whitish peripheral al. in press). Th ese prokaryotes grew in freshwater cortex composed of fi lamentous microorganisms ponds or in wet soil on the forest fl oor. (Girard et al. in press). Other abundant inclusions are short branched Several amber pieces had biofi lms of modern mi- fi lament-forming actinomycetes. Th e fi laments are croorganisms at their surface which were removed of c. 1 μm diameter and, at least two morphotypes using ultrasonic cleaning and decontaminating baths, are distinguishable. Th e most abundant, present in fi rst in 9-10% H2O2 then in 5% HF as described both outcrops, consists of fi laments with dichoto- by Girard et al. (2009a). Diff erent techniques were mous branching and forms microcolonies of up to used to investigate microorganisms: 30 μm diameter (Fig. 1A-C). No broken fi laments – Very small and thin fragments of amber were have been found here and therefore we assume that removed from larger pieces using a minute scalpel they grew in the liquid resin. Th e other morphotype and then mounted in Canada balsam or observed is characterised by fi laments with perpendicular in water on a microscopic slide. branching and associated spores (Fig. 1D, E). – Fragments containing arthropod inclusions were Occasionally, also rod-shaped bacteria (Fig. 2G) directly observed under the microscope in order and cyanobacterial fi laments (Fig. 1G, H) were not to destroy any fossils. found.

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AB CD

FGH

FIG. 1. — Prokaryotes found in Archingeay-Les Nouillers (ARC) and Cadeuil (CDL) ambers: A, B, microcolonies of actinomycetes with dichotomous branching; A, ARC115.22a; B, CDL2-107; C, detail of a single microcolony of Figure 1A (ARC115.22a); D, E, actinomycetes with perpendicular branching (ARC115.13a.2); F, sheathed ﬁ laments of cyanobacteria (ARC(1-1)c); G, ﬁ laments of a possible big cyanobacterium (CDL9L-e6); H, sheathed cyanobacterium (ARC111). Scale bars: A, B, 20 μm; C-E, H, 10 μm; F, 30 μm; G, 100 μm.

Diverse eukaryotes were found associated with Chlorococcaceae; Fig. 2G) has been found associ- these prokaryotes. Diﬀ erent occurrences of sep- ated with rod-shaped bacteria in Archingeay amber. tate hyphae show the presence of Ascomycota and Cadeuil amber provided a specimen of Enallax Basidiomycota (Fig. 2B). Some were preserved only napoleoni Girard, 2009 (Chlorococcales, Scenedes- as hyphae, and some other only as spores. Rare cases maceae; Girard 2009 this volume; Fig. 2H). of fungal fossils exhibiting both hyphae and spores in Few freshwater or soil-living testate amoebae and connection have been observed, sometimes forming possible cysts of those have been found in Archingeay dense mycelia. A dimorphic fungus forming mycelia amber. One taxon is morphologically similar to and yeast stages has been identiﬁ ed as a carnivorous modern specimens of Centropyxis discoides Ehrenberg, fungus (Ascomycota) based on the occurrence of hy- 1838 (Fig. 2I) and a second taxon to the rare modern phal rings as trapping devices (Schmidt et al. 2007). Leptochlamys ampullaria West, 1901. Nematodes which were found close to this fungus can be considered as its potential prey. ARBOREAL FUNGI AND PLANT REMNANTS Two taxa of freshwater green algae have been Apart from numerous stellate and pennate hairs found. A three-celled alga similar to the modern which probably originate from angiosperm trees genus Myrmecia Schreber, 1789 (Chlorococcales, of the amber forest, we found mycelia and single

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ABC

D EF

G H I

FIG. 2. — Selected eukaryotes found in Archingeay-Les Nouillers (ARC) and Cadeuil (CDL) ambers: A, aerial hyphae of a Metacapno- diaceae representative (ARC115.3); B, septate hyphae of ascomycetes or basidiomycetes (CDL2.31); C, septate hyphae forming arthrospores (ARC38M); D, germinating spore (CDL2-106); E, nematode (ARC149.7); F, fungal hyphae forming possible chlamydospores (CDL2-106); G, three-celled Myrmecia-like green alga (left) and rod-shaped bacteria (right) (ARC115.9); H, Enallax-like green alga (CDL26c); I, Centropyxis discoides-like testate amoeba (ARC115.21). Scale bars: A, 10 μm; B, 30 μm; C, H, I, 20 μm; D, F, G, 5 μm; E, 50 μm. hyphae of epiphytic fungi preserved in Archingeay shape. Some faecal pellets from Cadeuil amber, amber. Th ey represent the oldest known specimens however, might also provide evidence of arboreal of sooty moulds, an ecological group of ascomycetes fungi since they consist of septate hyphae. Peculiar which are specialized in inhabiting tree bark and setae and basidiospores found in Cadeuil amber twigs in humid environments. At a part of the myce- provide evidence of the presence of polypores grow- lium some aerial hyphae (Fig. 2A) are preserved. ing on the trees. Th e nearly globular shape of the hyphae and the ampullaceous apical dividing stages resemble those MARINE MICROORGANISMS of the modern family Metacapnodiaceae. Fossils of The most unusual discovery in the amber of sooty moulds were previously only known from Archingeay are marine microorganisms (Girard et Eocene Baltic and Oligocene Bitterfeld amber al. 2008, 2009b). Diverse centric diatoms (Fig. 3A, (Rikkinen et al. 2003). B, D) and other siliceous shells have been found in Insect excrements are not rare in the mid-Creta- several litter amber pieces sensu Perrichot (2004). ceous of southwestern France and they have largely Most diatoms have been found as inclusions of sin- been attributed to termites due to their general gle cells but chains of two or three cells also occur.

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ABC

D E F

FIG. 3. — Selected marine microorganisms found in Archingeay-Les Nouillers (ARC) amber: A, ﬁ liform centric diatom with a ring of spines (ARC115.11); B, centric diatom (ARC115.22); C, possible radiolarian (ARC115.2); D, centric diatom partially hidden by detritus (ARC115.11r); E, sponge spicule with central canal and a spiny surface (ARC115.12c); F, sponge spicule (ARC226.27). Scale bars: A, C, E, 5 μm; B, D, 10 μm; F, 50 μm.

Both morphological comparison to modern taxa of these arthropods and plants by the nematodes. and the known diatom fossil record suggest that Whether they were trapped together with their these diatoms are marine (Girard et al. 2009b). Th e host or independently on the forest fl oor or at a fi rst occurrence of non-marine diatoms comes from tree trunk is thus not determinable. the Maastrichtian of Mexico where an assemblage A well-preserved mycelium with hyphae forming of both centric and pennate diatoms was found arthrospores has been found in Archingeay amber (Chacón-Baca et al. 2002). Further marine amber (Fig. 2C). Th e hyphae are septate and composed inclusions are monoaxone sponge spicules, prob- of quadratic, elliptical and sub-spheroidal cells. ably of demosponges, occurring in the three dif- Th is specimen has been found on a fragment of ferent amber pieces from Archingeay-Les Nouillers wood embedded in amber, suggesting that it was (Fig. 3E, F) (Girard et al. 2008). A rounded siliceous a fungus growing either on the tree or on a wood inclusion, looking like a radiolarian, has also been fragment on the forest fl oor. First interpretation found in a piece of litter amber (Fig. 3C). shows that this fungus has similarities with some modern representatives of the Pleosporales (Asco- TERRESTRIAL MICROORGANISMS mycota) with spores resembling those of Valsaria OF UNKNOWN ORIGIN insitiva Ces. & De Not. Four diff erent kinds of nematodes have been found Th e prokaryotic inclusion shown in Figure 1G in Archingeay and Cadeuil amber (Fig. 2E). One was found in the central part of an amber piece of was attributed to litter environments (see above) Cadeuil, associated with wood debris and other and three other were found in amber pieces that sheathed prokaryotes. Th e cells appear to have a also contained both arthropods and plant debris. dark content and their shape and the growth form Th ese associations in amber could be accidental of the sheathed fi laments suggest a cyanobacterial and there is no direct evidence for any parasitism nature of the inclusion.

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FIG. 4. — Resinous forest of New Caledonia as a possible analogue to the Cretaceous amber forests of southwestern France: A, resinous forest of Araucaria columnaris (J.R.Forst.) Hook. growing directly at the coast of Maré, New Caledonia. The sea appears very calm because the island is protected by a coral reef; B, resin ﬂ ow on the bark of A. columnaris; C, resin dropping onto the forest ﬂ oor, a possible future piece of litter amber.

In the same locality, hyphae forming possible It was not possible to estimate where this fungal chlamydospores (Fig. 2F) have been found associ- inclusion was embedded in the resin (on the forest ated with remains of an undetermined arthropod. ﬂ oor or on the tree bark?).

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Several germinating spores (Fig. 2D) were found 2008). Sedimento logical and palaeontological data in Archingeay-Les Nouillers and Cadeuil amber. indicate that an estuarine area under warm and wet Without any diagnostic features, it was not possible climate existed in the Charentes region during the to attribute them to any group of fungi. mid-Cretaceous. Analyses of the arthropod inclusions as well as the wood fl ora associated with amber also support an estuarine to mangrove-like environment TAPHONOMY, PALAEOECOLOGY (Perrichot 2005; Perrichot et al. 2007). AND PALAEOENVIRONMENT AN ACTUALISTIC VIEW The taphocoenoses preserved in amber from Today it is hard to fi nd resinous conifer forests Archingeay-Les Nouillers and Cadeuil show in- close to coastal estuarine environments. But a view fl uences of both forest and marine habitats. Th e into the extensive Araucaria forests along the coast forestal representatives are dominated by litter of New Caledonia may help to comprehend the and soil microorganisms, especially by sheathed Charentes amber forest palaeoenvironment. Trees prokaryotes whose presence suggests that a large of Araucaria columnaris (J.R.Forst.) Hook. are of- quantity of resin was produced in humid environ- ten found standing directly at the sea shore on the ments, similar to modern coastal Taxodium swamps rocks of coral limestone (Fig. 4A). Since the New in Florida (Schmidt & Dilcher 2007). Caledonian coast is protected by a coral reef, even Th e diverse assemblage of soil and litter micro- dense forests of tall trees may grow in a coastal en- organisms (including cyanobacteria, bacteria, actino- vironment. Damage by fallen trees or branches, or mycetes, fungi, algae and testate amoebae) supports fi re may induce very extensive resin fl ow at the tree results previously obtained by the analysis of the trunks (Fig. 4B). Resin drops or, when produced arthropod fauna of Archingeay and Cadeuil am- at the base of tree trunks or by roots, fl ows at the ber. Perrichot (2004, 2005) introduced the term forest fl oor (Fig. 4B, C). Th ese resin fl ows then “litter amber” for pieces containing diverse litter- covers the litter horizon. dwelling arthropods. Two thirds of the arthropods Soil and litter-living organisms may become at- preserved in litter amber are dipterans; half of them tached to and enclosed by the resin fl ows. Bacteria are characteristic for litter habitats. Among the and fungi are often seen growing into resin as long other arthropods preserved, around 17% (includ- as it stays liquid (Schmidt & Dilcher 2007) and ing homopterans, heteropterans, springtails and may therefore become secondarily accumulated. isopods) are also typical litter-living organisms. Organisms or parts of those fallen from the trees Th e occurrence of actinomycetes and soil fungi in might become embedded at the upper side of the these litter amber pieces confi rms that particular resin pieces. Marine taxa or their shells might also resin pieces did not solidify on the tree bark, but get in contact with resin when blown by the wind on the forest fl oor. or spray at the resin bodies, or when previously Th e occasional occurrence of arboreal taxa, such introduced into the forest by high tides or storms as epiphytic fungi of the sooty moulds (Metacapno- before the resin fl ow occurred. diaceae) and plant remnants of stellate and pennate hairs, show that some of these particular pieces of resin were aerially secreted before solidifying on the CONCLUSION forest fl oor. Th us, resin dropping on the ground from the tree trunks (Fig. 4B, C) or resin produced Palaeoenvironments are often reconstructed with- by superfi cial roots can be assumed. out any data about microfauna and microfl ora, Forest and marine microorganisms are not prone the oldest organisms on earth and most important to be found as syninclusions in a single piece of am- part of modern ecosystems in term of diversity and ber and show that the amber forests were directly abundance. Th is important bias is mainly due to infl uenced by the marine environment (Girard et al. diff erential fossilization. Amber off ers a unique

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way to access fossil microorganism assemblages. “Interactions biodiversité végétale – changements Archingeay-Les Nouillers (Late Albian) and Cadeuil globaux à la transition Crétacé inférieur-supérieur (Late Albian-Early Cenomanian) ambers provides a d’Europe occidentale” and to the projet AMBRACE new window into this past micro-world. It reveals no. BLAN07-1-184190 from the Agence nationale that, during the mid-Cretaceous, amber forests de la Recherche (ANR). grew in coastal position in the Charentes region. Th ese amber forests had complex and diverse soil biocoenoses composed of cyanobacteria, bacteria, REFERENCES fungi, algae and testate amoebae. While arthropods preserved in these ambers are largely archaic repre- BRETON G. 2007. — La bioaccumulation de micro- sentatives, many microbes from the Cretaceous forest organismes dans l’ambre : analyse comparée d’un fl oor are morphologically close to modern species. ambre cénomanien et d’un ambre sparnacien, et Probably their microhabitats and their roles in the de leurs tapis algaires et bactériens. Comptes Rendus Palevol 6: 125-133. food web changed so little in Earth’s history that BRETON G. & TOSTAIN F. 2005. — Les microorganismes morphological changes were unnecessary. de l’ambre cénomanien d’Écommoy (Sarthe, France). One of the main characteristics of Archingeay Comptes Rendus Palevol 4: 31-46. and Cadeuil amber is that diff erent microcoenoses CHACÓN-BACA E., BERALDI-CAMPESI H., CEVALLOS- are preserved, sometimes in the same amber piece. FERRIZ S. R. S., KNOLL A. H. & GOLUBIC S. 2002. — 70 Ma nonmarine diatoms from northern Mexico. Interpreting the taphocoenosis of a single piece of Geology 30: 279-281. amber, one has to consider that the organisms may FLEURIAU DE BELLEVUE L. B. 1817. — Carte de l’île originate from very diff erent habitats, although d’Aix, de l’île d’Enet et de Fouras. Archives de la So- captured in the same taphotope. Archingeay-Les ciété des Sciences naturelles de Charente-Maritime 458 Nouillers amber provides the best evidence for (fonds Fleuriau). this. GALIPPE V. 1920. — Recherches sur la résistance des microzymas à l’action du temps et sur leur survi- vance dans l’ambre. Comptes Rendus de l’Académie des Sciences , Paris 170: 856-858. Acknowledgements GIRARD V. 2009. — Evidence of Scenedesmaceae (Chloro- We thank Simona and Jean-Paul Saint Martin phyta) from 100 million-year-old amber. Geodiversitas (Muséum national d’Histoire naturelle, Paris), 31 (1): 145-151. GIRARD V., SCHMIDT A. R., SAINT MARTIN S., STRUWE Heinrich Dörfelt (Institut für Geobotanik und S., PERRICHOT V., SAINT MARTIN J.-P., BRETON G. & Botanischer Garten, Halle) and Wilfried Schönborn NÉRAUDEAU D. 2008. — Evidence for marine micro- (Institut für Ökologie, Jena) for their help in the fossils from amber. Proceedings of the National Academy determination of some inclusions. We also thank of Sciences of the USA 105 (45):17426-17429. Kerstin Schmidt (Jena) and Saskia Jancke (Museum GIRARD V., NÉRAUDEAU D., BRETON G., SAINT MARTIN S. & SAINT MARTIN J.-P. 2009a. — Contamination für Naturkunde, Berlin) for improving the English of amber samples by recent microorganisms and of the manuscript. Jérôme Munzinger (Institut remediation evidenced by mid-Cretaceous amber of de Recherche pour le Développement, Nouméa) France. Geomicrobiology Journal 26 (1): 21-30. contributed by his knowledge of suitable sampling GIRARD V., SAINT MARTIN S., SAINT MARTIN J.-P., sites in New Caledonia. Th e fi eld studies in New SCHMIDT A. R., STRUWE S., PERRICHOT V., BRETON G. & NÉRAUDEAU D. 2009b. — Exceptional pres- Caledonia were kindly permitted by the Direction du ervation of marine diatoms in Upper Albian amber. développement économique et de l’environnement Geology 37 (1): 83-86. (Province nord) and by the Direction des Res- GIRARD V., BRETON G., BRIENT L. & NÉRAUDEAU D. sources naturelles (Province sud). Th e work on in press. — Sheathed prokaryotic fi laments, major resin-preserved microorganisms is supported by the components of mid-Cretaceous French amber microcoenoses. Journal of Paleolimnology: doi 10.1007/ German Research Foundation (DFG) and by the s10933-008-9287-2. Alexander von Humboldt Foundation. Th is article NÉRAUDEAU D., PERRICHOT V., DEJAX J., MASURE E., is a contribution to projects IFB Global Change NEL A., PHILIPPE M., MOREAU P., GUILLOCHEAU F. &

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GUYOT T. 2002. — Un nouveau gisement à ambre pterid bugs (Insecta: Heteroptera) in mid-Cretaceous insectifère et à végétaux (Albien terminal probable) : ambers from France and Myanmar (Burma). Palaeon- Archingeay (Charente-Maritime, France). Geobios tology 50: 1367-1374. 35: 233-240. RIKKINEN J., DÖRFELT H., SCHMIDT A. R. & WUNDER- NÉRAUDEAU D., PERRICHOT V., COLIN J.-P., GIRARD V., LICH J. 2003. — Sooty moulds from European Ter- GOMEZ B., GUILLOCHEAU F., MASURE E., PEYROT D., tiary amber, with notes on the systematic position TOSTAIN F., VIDET B. & VULLO R. 2008. — A new of Rosaria (“Cyanobacteria”). Mycological Research amber deposit from the Cretaceous (Upper Albian- 107: 251-256. Lower Cenomanian) of SW France. Cretaceous Research SCHLÜTER T. 1978. — Zur Systematik und Palökologie 29 (5-6): 925-929. harzkonservierter Arthropoda einer taphozönose aus NÉRAUDEAU D., VULLO R., GOMEZ B., GIRARD V., LAK dem Cenomanium von N-W Frankreich. Berliner M., VIDET B., DEPRÉ E. & PERRICHOT V. 2009. — Geowissenchaftliche Abhandlungen (A) 9: 1-150. Amber, plant and vertebrate fossils from the Lower SCHMIDT A. R. & DILCHER D. L. 2007. — Aquatic Cenomanian paralic facies of Aix Island (Charente- organisms as amber inclusions and examples from Maritime, SW France). Geodiversitas 31 (1): 13-28. a modern swamp forest. Proceedings of the National PERRICHOT V. 2004. — Early Cretaceous amber from Academy of Sciences of the USA 104: 16581-16585. south-western France: insight into the Mesozoic litter SCHMIDT A. R., DÖRFELT H. & PERRICHOT V. 2007. — fauna. Geologica Acta 2: 9-22. Carnivorous fungi from Cretaceous amber. Science PERRICHOT V. 2005. — Environnements paraliques 318: 1743. à ambre et à végétaux du Crétacé nord-aquitain VULLO R. 2007. — Les vertébrés du Crétacé supérieur (Charentes, Sud-Ouest de la France). Mémoires de des Charentes (Sud-Ouest de la France) : biodiversité, Géosciences Rennes 118: 1-310. taphonomie, paléoécologie et paléobiogéographie. PERRICHOT V., NEL A. & NÉRAUDEAU D. 2007. — Schizo- Mémoires de Géosciences Rennes 125: 1-357.

Submitted on 4 January 2008; accepted on 4 September 2008.

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