Testate Amoebae from a Cretaceous Forest Floor Microbiocoenosis of France

ALEXANDER R. SCHMIDT,a VINCENT GIRARD,b,c VINCENT PERRICHOTb,d and WILFRIED SCHONBORNe

aCourant Research Centre Geobiology, Georg-August-Universitat Gottingen, Goldschmidtstrasse 3, D-37077 Gottingen, Germany, andbUniversite de Rennes 1, Unite Mixte de Recherche Centre National de la Recherche Scientifique 6118, 263 avenue du General Leclerc,

F-35042 Rennes Cedex, France, andcDepartment of Biology, Dalhousie University, Halifax, NS B3H 4J1, Canada, and

dPaleontological Institute, University of Kansas, Lindley Hall, 1475 Jayhawk Boulevard, Lawrence, Kansas 66045, USA, andeFriedrich-Schiller-Universitat Jena, Institut fur Okologie, Dornburger Strasse 159, D-07743 Jena, Germany

ABSTRACT. Amber-preserved shells of testate amoebae often provide as many diagnostic features as the tests of modern taxa. Most ofthese well-preserved microfossils are morphologically assignable to modern species indicating either evolutionary stasis or convergentevolution. Here we describe two Lower Cretaceous testate amoebae that are clearly distinguishable from modern species. Centropyxisperforata n. sp. and Leptochlamys galippei n. sp. possessed perforate shells that were previously unknown in these genera. They arepreserved in highly fossiliferous amber pieces from the Upper Albian (ca. 100 million years old) of Archingeay/Les Nouillers (Charente-Maritime, southwestern France). Syninclusions of soil and litter dwelling arthropods and microorganisms indicate a limnetic-terrestrialmicrohabitat at the floor of a coastal conifer forest.

Key Words. Amber, Arcellinida, Centropyxis, fossil microorganisms, Leptochlamys, palaeoecology, testate lobose amoebae.

SHELLS of testate amoebae are only rarely well-preserved inProterozoic to Cenozoic sediments (e.g. Foissner and Schiller

2001; Porter and Knoll 2000; van Hengstum et al. 2007). In thelast two decades, finds in Triassic to Neogene fossil resins pro-vided new insights into the evolutionary history of various test-acean families (see Schmidt, Schonborn, and Schafer 2004;Schmidt et al. 2006; Waggoner 1996a, b). The families Centro-pyxidae, Difflugiidae, Hyalosphenidae, and Phryganellidae (orderArcellinida) are especially represented in fossil resins. Amber-preserved shells of these testate amoebae often provide as manydiagnostic features as do the tests of modern taxa. Most of thesewell-preserved microfossils are morphologically assignable tomodern species indicating either evolutionary stasis or conver-gent evolution.

Investigating highly fossiliferous amber pieces from the Albianof southwestern France, we found two new taxa of testate amoe-bae that are associated with various litter- and soil-living arthro-pods and microorganisms. The specimens are assignable to therecent genera Centropyxis and Leptochlamys but distinguishedfrom extant species by the occurrence of minute perforations inthe shells. Therefore, we describe the new fossil species Centro-pyxis perforata n. sp. and Leptochlamys galippei n. sp.

MATERIALS AND METHODS

The amber pieces that contain the fossil amoebae shells werefound in the quarry of Archingeay/Les-Nouillers in Charente-Maritime, southwestern France. The amber is derived from alter-nating layers of estuarine sand and clay containing mixedfragments of fossil plants (e.g. cuticles and lignitic wood). Inthe regional stratigraphical section, this amber-bearing stratumcorresponds to the lithological subunit A1 sensu Neraudeau andMoreau (1989) and was dated as Upper Albian (ca. 100 millionyears old) by palynological studies (Dejax and Masure 2005;Neraudeau et al. 2002).

The ground and polished amber pieces were investigated usinga Nikon Optiphot II transmitted-light microscope (Nikon Cor-poration, Tokyo, Japan), equipped with a Canon 300D digitalcamera (Canon Inc., Tokyo, Japan). The amber clasts containing

the fossil amoebae shells are deposited in the amber collections ofthe Department of Geosciences of the University Rennes 1,France (labelled ‘‘IGR’’), and the Department of Earth History,Museum National d’Histoire Naturelle, Paris (labelled‘‘MNHN’’). Amber fragment number ARC-115.21b that containsthe Centropyxis shells is a part of the MNHN palaeoentomologicalcollection since it contains the holotype and allotype of Eophle-botomus carentonensis, which are dipterans of the family Psy-chodidae (Azar et al. 2003); those insect types are recorded underthe collection numbers MNHN A30167 and MNHN A30168, re-spectively). The original amber piece number ARC-115 was4 � 3 � 2 cm in size, but it has been divided into 39 fragmentsin order to investigate the numerous inclusions (preparation afterPerrichot 2004). Amber piece number IGR-ARC-386 that is about1 � 1 � 1 cm in size contains the Leptochlamys shell. The amberfragments number IGR-ARC-60.4 and IGR-ARC-263.15 (coll. A.Gaugain) contain the numerous possible resting stages of testateamoebae. Since the two original pieces ARC-60 and ARC-263contained numerous arthropods, they were also divided in severalfragments to separate the inclusions.

Requests for examination of the material should be addressedonline at http://colhelper.mnhn.fr/ or directly to V.P. (vincent.perrichot@univ-rennes.fr).

RESULTS

Inclusions of the genus Centropyxis. Two brownish testaceanshells of �50mm diameter are preserved in the amber fragmentARC-115.21b. The description, however, is based solely on the il-lustrated specimen (Fig. 1–3, 12–13). In the second shell, the rele-vant features are not accessible because it is surrounded by detritusparticles. The exposed shell is slightly damaged laterally (black ar-row in Fig. 2) and an elongate acuminate structure of �500mmlength (arrow in Fig. 1) extends through the amber matrix. Thisstructure possibly represents fossilized cell plasma that flowed out ofthe broken shell when it was moved by the flowing viscose resin.Based on its shape and colour (Fig. 1–3, 12–13) the fossil is a typicalCentropyxis shell. However, the shell possesses six pores of �3mmdiameter, which are atypical for extant representatives of this genusand on which basis we describe a new species.

Order Arcellinida Kent 1880Family Centropyxidae Jung 1942Genus Centropyxis Stein 1859Centropyxis perforata A.R. Schmidt, Girard et Schonborn

n. sp. (Fig. 1–3, 12–13)

Corresponding Author: A. R. Schmidt, Courant Research CentreGeobiology, Georg-August-Universitat Gottingen, Goldschmidtstrasse3, D-37077 Gottingen, Germany—Telephone number: 149 551397957; FAX number: 149 551 397918; e-mail: alexander.schmidt@geo.uni-goettingen.de

245

J. Eukaryot. Microbiol., 57(3), 2010 pp. 245–249r 2010 The Author(s)Journal compilation r 2010 by the International Society of ProtistologistsDOI: 10.1111/j.1550-7408.2010.00471.x

Published bythe International Society of ProtistologistsEukaryotic Microbiology

The Journal of

Diagnosis. The brown circular shell is 48mm in diameter andnot covered by xenosomes. The nearly central aperture is circular,slightly invaginated and 14 mm in diameter. The shell surface isrough. In the ventral region, four pores of � 3mm diameter sur-round the aperture about 7–10 mm from it (Fig. 2, 12). Two poresof the same size are located at the dorsal side (Fig. 3, 12). As in theaperture, the shell is also slightly invaginated around the pores.Analysis of different optical sections suggests that the shell prob-ably is discoid in lateral view (Fig. 13).

Type location. Upper Albian (ca. 100 million years old) amberfrom the quarry of Archingeay/Les-Nouillers, Charente-Maritime,southwestern France.

Type material. The holotype as shown in Fig. 1–3 is depositedin the amber collection of the Department of Earth History,

Museum National d’Histoire Naturelle, Paris; collection numberMNHN A31889.

Etymology. The specific epithet refers to the pores in the dor-sal and ventral region of the shell.

Discussion. We assume that the new fossil species is closelyrelated to the extant species Centropyxis discoides (Penard, 1890)Deflandre, 1929. Shape, colour, and surface of the shell as well asthe aperture are very similar to this extant species. However,C. discoides is significantly bigger, showing a size range from 150to 240 mm. The pores in the ventral and dorsal region are uniquefeatures of the fossil and the reason for the description of a newspecies. These pores are different to those of the modern genusArcella in which the pores have a regular distance from the ap-erture. The pores of the fossil are bigger and less numerous than in

Fig. 1–11. Photomicrographs showing the testate amoebae from Upper Albian amber of Archingeay/Les Nouillers (Charente-Maritime, southwest-ern France). 1–3. Holotype of Centropyxis perforata n. sp. (ARC-115.21b, collection number MNHN A31889). 1. Shell of C. perforata n. sp. in ventralview in the lower left-hand corner. The arrow indicates the elongate acuminate structure that possibly represents fossilized cell plasma that flowed out ofthe broken shell. A part of an enclosed dipteran of the family Psychodidae is visible at the right. 2. Ventral view of C. perforata n. sp. Rough shell surface,aperture, and four ventral pores are visible. The white arrow indicates a poorly visible pore; the black arrow indicates the broken part of the shell.3. Dorsal view of C. perforata n. sp. Both dorsal pores are indicated by arrows. 4–7. Holotype of Leptochlamys galippei n. sp. (IGR-ARC-386) in fouroptical sections. 4. Overview of L. galippei n. sp. 5. One pore of L. galippei n. sp. in focus (arrow). 6. Dorsal part of L. galippei n. sp. with indentation infocus. 7. Ventral part of L. galippei n. sp. with aperture in focus. Note that the granules visible in Fig. 5 and 7 are structures of the fossil resin; they are notattached to the shell surface. 8–11. Possible resting stages of testate amoebae in amber piece IGR-ARC-60.4 and IGR-ARC-263.15. 8. Five inclusionsclose to each other. Further dark structures that probably represent detritus are attached to some of the inclusions (IGR-ARC-263.15). 9–11. Singleinclusions with dark content, possibly resting cysts (Fig. 9: IGR-ARC-263.15; Fig. 10–11: IGR-ARC-60.4). Scale bars 5 20mm.

246 J. EUKARYOT. MICROBIOL., 57, NO. 3, MAY–JUNE 2010

Arcella. Since the fossil shell is slightly invaginated around thepores, the pores can be considered as a shell feature, not as frac-tures or artefacts formed during embedding or fossilization. Untilnow, pores are unknown in the shells of the genus Centropyxis.Only the related extant genus Bullinularia (e.g. B. indica (Penard,1907) Deflandre, 1953) has pores near the aperture. Internal pillarsare sometimes possessed in Centropyxis shells to support the dor-sal shell surface; minute pore-like depressions may then occur atthe attachment sites of these pillars at the dorsal side of the shell(Ogden 1988). In contrast, the fossil does not possess pillars andthe pores occur at both sides of the shell.

Inclusion of the genus Leptochlamys. The balloon-shapedtranslucent shell in amber fragment IGR-ARC-386 is � 60mm insize and slightly indented dorsally (Fig. 4–7, 14). This damagepossibly happened during embedding in the resin. This fossil shellresembles the rare modern and previously monotypic genusLeptochlamys, which, however, does not possess pores.

Order Arcellinida Kent 1880Family Hyalosphenidae Schultze 1877Genus Leptochlamys West 1901Leptochlamys galippei A.R. Schmidt, Girard et Schonborn

n. sp. (Fig. 4–7, 14)Diagnosis. The translucent unstructured shell is balloon-

shaped and circular in transverse section. It is � 60 mm in heightand the maximum diameter is � 55 mm. The terminal aperture iscircular and 12 mm in diameter. A slight formation of a collar isvisible (Fig. 7). Two opposite pores of 2–3mm are visible in theshell (see Fig. 5).

Type location. Upper Albian (ca. 100 million years old) amberfrom the quarry of Archingeay/Les-Nouillers, Charente-Maritime,southwestern France.

Type material. The holotype as shown in Fig. 4–7 is depositedin the amber collection of the Department Geosciences, Univer-sity Rennes 1, France; collection number IGR-ARC-386.

Etymology. Named in honour of M.V. Galippe, the firstFrench researcher who investigated microorganisms obtainedfrom amber. Galippe (1920) described modern (not fossil) mi-crobes that he cultivated from the surface and fissures of variousMesozoic and Cenozoic amber pieces.

Discussion. The fossil is very similar to the extant speciesLeptochlamys ampullacea West, 1901, which also has a balloon-shaped shell up to 55 mm in height and 48mm in diameter. Theunique features and the reason for the description of a new speciesare the pores. Pores of opposite arrangement occur also in someextant testacean shells. This suggests that the pores of the fossilare natural and no artefacts of fossilization. Leptochlamys amp-

ullacea is a very rare species that was found in limnetic habitats.The assignment of this microfossil to the modern genus Leptochl-amys is based on the shell morphology only since pseudopodia arenot visible in fossil testate amoebae. Recent Leptochlamys spec-imens have lobose pseudopodia, which are not preserved in fos-sils. Among the extant testate amoebae Leptochlamys is the onlygenus with such a shell-type and therefore unmistakable.

Further possible inclusions of testate amoebae. About 150organismic inclusions of 30–52-mm size are located close to eachother in two different amber pieces (IGR-ARC-60.4 and IGR-ARC-263.15 (coll. A. Gaugain); Fig. 8–11). According to the shape andsurface structure they might represent lobose testate amoebae, too.However, an opening is not, or at least not clearly, visible in thesemicrofossils. Possibly, these inclusions represent resting stages.Similar structures were illustrated and described as cysts ofmodern specimens of the genus Phryganella by Valkanov (1963).

DISCUSSION

Palaeoecology. Mixed coastal forests dominated by the coniferfamilies Araucariaceae and Cheirolepidiaceae at the eastern rimof the young Atlantic Ocean were the amber source (Peyrot, Jolly,and Barron 2005). The reconstruction of the depositional envi-ronment (Perrichot 2005; Perrichot, Nel, and Neraudeau 2007a)and the occurrence of marine microorganisms in some amberpieces (Girard et al. 2008) revealed that these forests grew close tothe seashore, most probably in an estuarine environment. Numer-ous inclusions of arthropods and microorganisms have been de-scribed from this locality (for review, see Girard et al. 2009b;Perrichot and Girard 2009; and Perrichot et al. 2007b). The test-aceans originally fossilized in highly fossiliferous pieces of am-ber. For example, 79 arthropods and numerous microorganisms,such as bacteria, algae, and carnivorous fungi, are preserved inamber piece ARC-115 (Perrichot and Girard 2009). Most of theseorganisms, such as schizopterid bugs (Perrichot et al. 2007a), amole cricket (Perrichot et al. 2002), and a tanaupodid mite (Judsonand Makol 2009), belong to biocoenoses of the humid litter andsoil habitats of the forest floor. This shows that the highly fossil-iferous amber piece likely solidified on the forest floor rather thanon the tree bark (Girard et al. 2009b).

Fig. 12–13. Diagrammatic drawings of Centropyxis perforata n. sp.12. Ventral view with four ventral pores around the aperture. The twodorsal pores are indicated by dotted circles. 13. Supposed dorsoventralsection of the shell. Scale bars 5 10 mm.

Fig. 14. Diagrammatic drawing of Leptochlamys galippei n. sp. inlateral view. Scale bar 5 10 mm.

247SCHMIDT ET AL.—CRETACEOUS TESTATE AMOEBAE

Among the microorganisms, decomposers were the most abun-dant ecological group in the ‘‘litter amber’’; they are representedby at least three taxa of actinomycetes, various fungi, and nem-atodes. Also, rod-shaped bacteria and sheathed cyanobacteria(Girard et al. 2009a, b) were frequently enclosed. Among thefungi, the most remarkable species is a carnivorous fungus, whichpossessed trapping rings and yeast stages (Schmidt, Dorfelt, andPerrichot 2007, 2008). Its yeast stage is most likely related tolimnetic microhabitats at the forest floor. Cyanobacteria and greenalgae of the genus Enallax and a Myrmecia-like specimen belongto the primary producers in this microbiocoenosis and probablyalso lived in limnetic or limnetic-terrestrial microhabitats (Girard2009; Girard et al. 2009b). Our newly discovered protozoans be-long to the consumers in this ancient microbial food web. Testateamoebae prey on bacteria and microalgae and they participate to ahigh degree in secondary production and, therefore, in the turn-over of matter. We assume that the newly discovered Centropyxisand Leptochlamys species settled in limnetic microhabitats liketheir modern relatives C. discoides and L. ampullacea.

The Mesozoic fossil record of testate amoebae. Freshwatertestate amoebae of the families Centropyxidae and Difflugiidaehave been recorded from non-marine habitats since the Carnian(Schmidt et al. 2006) and of the families Hyalosphenidae andPhryganellidae since the Early Cretaceous (Schmidt et al. 2004;Schonborn et al. 1999; van Hengstum et al. 2007). Older reportsfrom non-marine environments are doubtful (for review, see Med-ioli et al. 1990b and Schmidt et al. 2004). Most Mesozoic amberinclusions of testacean shells are morphologically indistinguish-able from extant species. Examples from amber are Centropyxishirsuta from the Carnian of Italy (Schmidt et al. 2006), Nebela cf.tubulata Brown, 1911 from the Albian-Cenomanian of Kansas(Waggoner 1996a), and Centropyxis aculeata Deflandre, 1929,Centropyxis delicatula Penard, 1902, C. hirsuta Deflandre, 1929,Cyclopyxis eurystoma Deflandre, 1929, Phryganella acropodia(Hertwig & Lesser, 1874) Penard, 1902, and Phryganella para-doxa Penard, 1902 from the Cenomanian of Germany (Schmidtet al. 2004; Schonborn et al. 1999; see Schmidt, von Eynatten, andWagreich 2001 for dating of this German amber, which had beenconsidered to be Triassic in age in the 1990s).

Outside fossil resins, most Mesozoic testate amoebae are lesswell preserved. Medioli, Scott, and Wall (1990a) described thefamilies Centropyxidae, Difflugiidae, and Hyalosphenidae fromLower Albian freshwater deposits in Canada. Recently, Bassiet al. (2008) reported poorly preserved microfossils from Juras-sic sediments of Italy, which they assigned to the genera Centro-pyxis, Difflugia, and Pontigulasia. However, current finds ofAlbian testaceans, which fossilized in sediments in excellent con-dition (van Hengstum et al. 2007), confirm our results obtainedfrom amber: Mesozoic specimens are largely indistinguishablefrom modern species. These authors found many specimens of thefamilies Difflugiidae and Hyalosphenidae, which were assignableto modern species, although a high intraspecific variability wasobserved. The assemblages included the species Difflugia oblongaEhrenberg, 1832, Difflugia protaeiformis Lamarck, 1816, Difflu-gia urens Patterston et al. 1985, Pontigulasia cf. compressa(Carter, 1864) Rhumbler, 1895, Lagenodifflugia cf. vas (Leidy,1874) Medioli & Scott, 1983, Cucurbitella tricuspis (Carter,1856) Medioli, Scott & Abbott 1987, and Lesquereusia spiralis(Ehrenberg, 1840) Schlumberger, 1845. Only one new species,Difflugia baukalabastron van Hengstum et al. 2007, could be dis-tinguished by these authors.

Comparing these Mesozoic fossils to extant species, one mustconsider the possibility of convergent evolution. However, thelargely asexual reproduction of testate amoebae could explain thisunusual evolutionary stasis over some 100 million years. At least,

the fossil record revealed that representatives of the families Cen-tropyxidae, Difflugiidae, Hyalosphenidae, and Phryganellidaecolonized Mesozoic limnetic and limnetic-terrestrial microhabi-tats in high diversity (Medioli et al. 1990a; Schmidt et al. 2004,2006; Schonborn et al. 1999; van Hengstum et al. 2007; Wag-goner 1996a). It is especially remarkable that all known Mesozoicrepresentatives are testaceans with organic shells and mostly withcovering xenosomes. However, wet habitats are today colonizedin particular by large numbers of taxa with shells consisting ofsiliceous idiosomes (especially Euglyphidae). These taxa have notbeen recorded from deposits older than Middle Eocene (Schiller1998, 1999) and the only amber-preserved specimen of this groupso far is a Cyphoderia-like inclusion from the Miocene Dominicanamber (Waggoner 1996b). Only recently, the genera Assulina,Cyphoderia, and Trinema of the Testaceafilosia have been re-ported from the Lower Cretaceous Alava amber of Spain (Martın-Gonzalez et al. 2009). However, these 114 million-year-old in-clusions look very strange and do not withstand a critical exam-ination. No essential diagnostic features, such as an aperture, astructured shell, or idiosomes, are visible in the illustrations pro-vided by these authors. Thus, we postulate that this study dealswith structures of the resin itself that can be abundantly observedin modern tree resins and ambers (Schmidt 2003; Schmidt et al.2004).

ACKNOWLEDGMENTS

The authors thank Kerstin Schmidt (Jena) for critical remarkson the manuscript and Dany Azar (Fanar-Matn and Paris), GerardBreton (Rennes), Didier Neraudeau (Rennes), and Steffi Struwe(Berlin) for advice. Arnaud Gaugain (Coye-la-Foret) kindly pro-vided one amber piece with possible testacean amoebae discussedherein. This is Publication number 21 from the Courant ResearchCentre Geobiology that is funded by the German Initiative of Ex-cellence. V.G. acknowledges support by the ‘‘Declics-Jeunes’’from the French Foundation (Fondation de France). This study is acontribution to the project AMBRACE (BLAN07-1-184190) ofthe French National Research Agency.

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Received: 08/29/09, 01/13/10; accepted: 01/14/10

249SCHMIDT ET AL.—CRETACEOUS TESTATE AMOEBAE