| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
(American Journal of Botany. 2008;95:1328-1334.) doi: 10.3732/ajb.0800143 © 2008 Botanical Society of America, Inc. |
What's this? |
Brief Communication |
2 Georg-August-Universität Göttingen, Courant Research Centre Geobiology, Goldschmidtstrasse 3, 37077, Göttingen, Germany 3 Museum für Naturkunde der Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115 Berlin, Germany 4 Martin-Luther-Universität Halle, Institut für Geobotanik und Botanischer Garten, Neuwerk 21, 06108 Halle/Saale, Germany 5 Paleontological Institute, University of Kansas, Lindley Hall, 1475 Jayhawk Blvd, Lawrence, Kansas 66045 USA
Received for publication 22 April 2008. Accepted for publication 8 August 2008.
ABSTRACT
In habitats where nitrogen is the limiting factor, carnivorous fungi gain an advantage by preying on nematodes and other microorganisms. These fungi are abundant in modern terrestrial ecosystems, but they are not predestined for preservation as fossils. Conclusions on their evolutionary history are therefore mainly based on molecular studies that are generally limited to those taxa that have survived until today. Here we present a fossil dimorphic fungus that was found in Late Albian amber from southwestern France. This fungus possessed unicellular hyphal rings as trapping devices and formed blastospores from which a yeast stage developed. The fossil probably represents an anamorph of an ascomycete and is described as Palaeoanellus dimorphus gen. et sp. nov. Because predatory fungi with regular yeast stages are not known from modern ecosystems, the fungus is assumed to not be related to any Recent carnivorous fungus and to belong to an extinct lineage of carnivorous fungi. The inclusions represent the only record of fossil fungi that developed trapping devices, so far. The fungus lived c. 100 million years ago in a limnetic-terrestrial microhabitat, and it was a part of a highly diverse biocenosis at the forest floor of a Cretaceous coastal amber forest.
Key Words: amber • carnivorous fungi • Deuteromycotina • fossil fungi • nematophagous fungi • Palaeoanellus dimorphus • paleoecology • paleomycology
Carnivory in plants and fungi is interpreted as an adaptive trait in habitats where relevant nutrients are scarce. Carnivorous plants typically capture, kill, and digest arthropods, whereas carnivorous or predatory fungi prey on nematodes and other microorganisms. Fungi are very important decomposers in forestal ecosystems; however, nitrogen that is essential to fungal growth is not freely available in dead wood or forest soils. Because of the very high carbon to nitrogen ratio of wood, nitrogen is the limiting factor for the growth of wood-decaying fungi. In such nutrient-poor habitats, direct assimilation of nitrogen compounds from animals is considered to be an advantage (Barron, 2003
).
Carnivorous fungi prey facultatively on amoebae, nematodes, rotifers, springtails, and many other small terrestrial or aquatic animals (Barron, 1977; Dove, 1987). This carnivorous mode of life is known from more than 200 species of Recent fungi (Li et al., 2000; Yang et al., 2007). They belong to the Saprolegniales (Oomycetes), Zoopagales (Zygomycetes), and to imperfect (anamorphic) stages of the Ascomycetes and Basidiomycetes. These fungi developed distinctive morphological structures for trapping animals. Simple adhesive hyphae and spores are able to capture the prey, but there are also specialized adhesive hyphal branches, sessile and stalked adhesive knobs, adhesive networks, and constricting or nonconstricting rings (Dove, 1987). Different trapping devices may occur in a single species, and the combination of adhesive knobs and nonconstricting rings has been known for a long time (e.g., Drechsler, 1934, 1950). Trapped animals are the main nutritional source for the predatory fungi. In most species, however, predation is combined with a saprotrophic mode of nutrition. Sometimes mycoparasitism was also observed in carnivorous fungi (e.g., Li et al., 2003).
We found many inclusions of a fungus that developed hyphal rings as trapping devices by investigating microinclusions in c. 100 million-year-old Cretaceous amber from southwestern France. Based on the mode of ring formation and the dimorphic mode of life, the fossils are not assignable to any modern carnivorous fungus. It is the intent of this study to describe the fossil carnivorous fungus reported by Schmidt et al. (2007) in detail and to discuss more extensively its paleoecology and mode of life.
MATERIALS AND METHODS
The amber piece number ARC115 that contains the fossil fungus was found in the quarry of Archingeay/Les-Nouillers in Charente-Maritime (southwestern France). Numerous inclusions of arthropods have been described from this locality (see Perrichot et al., 2007b, for review). The amber was found in alternating layers of estuarine sand and clay containing mixed fragments of fossil plants (cuticles and lignitic wood). In the regional stratigraphical section, this amber-bearing stratum corresponds to the lithological subunit A1 sensu Néraudeau and Moreau (1989) and was dated as Late Albian (c. 100 million years old) by palynological studies (Néraudeau et al., 2002; Dejax and Masure, 2005).
The original 4 x 3 x 2 cm piece of amber was divided into 31 pieces to separate the inclusions for investigation. This preparation followed the method described by Perrichot (2004). The ground and polished amber pieces were investigated using transmitted-light microscopes (Nikon Optiphot II, Nikon Corporation, Tokyo, Japan, equipped with a Canon 300D digital camera, Canon Inc., Tokyo, Japan). To better illustrate the three-dimensional oriented inclusions, we combined some photomicrographs using the program HeliconFocus 4.45. Figures 1B, 2E, H, I, 3A, B, and E–G were obtained from two optical sections, Figs. 1C, 2A, and J from three, and Fig. 3I from five.
|
|
|
RESULTS
Amber piece number MNHN ARC115.13 contains a fragment of decomposed wood with a mycelium and the trapping ring shown in Figs. 1A and 2A, as well as dispersed yeast cells and several nematodes. MNHN ARC115.22a contains a mycelium with two trapping rings and yeast cells (Figs. 1B, 2B, F). Some detritus or remnants of prey are visible in one ring (Figs. 1B, 2B). The second ring is still attached to a supporting hypha and is covered by tiny detritus particles (Fig. 2F). Syninclusions in this amber fragment are diatoms of the genera Hemiaulus and Stephanopyxis, scales of Lepidoptera wings, and legs of arthropods. MNHN ARC115.20 yields mycelia as well as a loop representing an initial stage of ring formation (Fig. 2C). Attached to a piece of detritus, several hyphae that form blastospores and secondary spores are preserved (Figs. 1C, 2J). Many yeast colonies are also preserved (Fig. 3A, B, F), some of which are still connected to hyphae (Fig. 3A, B). Syninclusions are a dipteran, a fragment of a hymenopteran, and a radiolarian. MNHN ARC115.5a contains a mycelium in which some hyphae form blastospores (Fig. 2H, I). Numerous small yeast colonies (Figs. 1D, 3E, G, I) are located close to the hyphae. Several nematodes and a dipteran were found as syninclusions. MNHN ARC115.13a contains an isolated ring that is visible in detritus (Fig. 2E). Syninclusions are numerous Actinomycetes and a diatom resembling the genus Cyclotella. MNHN ARC115.25 contains a ring that is attached to detritus.
SYSTEMATICS
Subdivision: Deuteromycotina (anamorphic fungi)
Genus: Palaeoanellus Schmidt, Dörfelt, et Perrichot gen. nov.
Generic diagnosis
Fungi dimorphi cum altera forma filamentosa (forma hypharum), cum altera forma prolificatione cellularum (forma faecis). Ad hyphae anelli nati sunt. Cellulae prolificationis apicaliter et lateraliter ortae sunt ex hyphis. Genus solum nodum est fossile. Formatio anelli non concordat cum formatio anelli recentibus vermes captantibus fungis. Anelli possident solum septum et sine petiolo. Typus generis: Palaeoanellus dimorphus.
Type species: Palaeoanellus dimorphus Schmidt, Dörfelt, et Perrichot sp. nov. (Figs. 1–3)
Specific diagnosis
Fungus fossilis in resina cretaceorum stratorum. Hyphae crassae circa 2 µm, hae anelli faciunt cum diametro circa 11–15 µm. Blastosporae (cellulae proliferatione) et cellulae faecis ellipsoides usque ovati et granditas est circa 2.5–3.5 x 3.5–5 µm, cum apicalibus et lateralibus germinatibus cellulis, hae cellulae formant faex. Holotypus: Collectio numerus MNHN ARC115.13; Museum naturalis Parisiis.
Holotype
MNHN ARC115.13 Muséum National d’Histoire Naturelle (MNHN), Paris (Figs. 1A, 2A).
Paratypes
MNHN ARC115.22a (paratype 1, Figs. 1B, 2B, F.), MNHN ARC115.20 (paratype 2, Figs. 1C, 2C, J, 3A, B, F).
Additional specimens
MNHN ARC115.5a (Figs. 1D, 2H, I, 3E, G, I); MNHN ARC115.13a (Fig. 2E); MNHN ARC115.25.
Locality
Quarry of Archingeay/Les-Nouillers, Charente-Maritime, southwestern France.
Age and stratigraphy—Late Albian (c. 100 million years), lithological subunit A1 sensu Néraudeau and Moreau (1989).
Etymology
The generic name is composed of the Greek word "palaiós" for "ancient, old" and the Latin word "anellus" for "small ring." The specific epitheton refers to the dimorphic mode of life of the fungus (dimorph = with two morphs).
Description
The mycelium consists of irregularly septated branched hyphae that are mostly 1.5–2.5 µm in diameter (Figs. 1A–C, 2H–J). The smallest hyphae are 1 µm in diameter, and rarely the hyphae reach up to 3 µm diameter. The rings originate from c. 2-µm-thick lateral branches of the hyphae, which form a loop. An initial stage of ring development is shown in Figs. 2C and D. The rings are unicellular, forming a single septum at the junction (Figs. 2B, G). Five rings were found, and their inner diameter ranges between 8–11 µm, their outer diameter being between 11–15 µm (Table 1). Fully developed rings probably detached easily from the supporting hypha and are also found disassociated from the mycelium (Fig. 2E). Because of sometimes numerous adhered particles (Fig. 2F), we assume that these rings produced a sticky secretion, improving the efficiency of trapping, as known from modern carnivorous fungi trapping using adhesive networks or knobs.
|
The blastospores and budding cells of the yeast stage are c. 2.5–3.5 x 3.5–5 µm in size. Large cells reach up to c. 3–4 x 4–6 µm. Width in relation to length ranges largely between 1:1.3–1.5, rarely reaching 1:2. Smaller budding cells were probably embedded in the liquid resin when growing. These cells are therefore sometimes more elongated, reaching a width-to-length ratio of 1:2–1:2.2. Even longer cells that are seen in some yeast colonies are interpreted as formation of new hyphae (Fig. 3I, J).
DISCUSSION
Systematic evaluation
Carnivorous fungi of modern ecosystems are polyphyletic. They occur in the Saprolegniales (Oomycetes), Zoopagales (Zygomycetes), and in anamorphs of the Ascomycetes and Basidiomycetes. This polyphyly shows that ecological adaptations led independently to similar structures in a convergent development (Dove, 1987; Liou and Tzean, 1997; Barron, 2003). Some taxa were able to highly diversify because of their successful carnivorous mode of nutrition. The wealth of anamorphs such as Arthrobotrys, Dactylaria, Dactylella, and Monacrosporium, which are assignable to the genus Orbilia (Ascomycetes), is an example of this (see Drechsler, 1950; Pfister, 1997; Ahren and Tunlid, 2003; Li et al., 2005, Yang et al., 2007).
It is very likely that during Earth’s history, carnivorous soil fungi also occurred in other groups and possessed analogous trapping devices. However, so far, there is only one report of possible nematophagous fungi: Jansson and Poinar (1986) described fungal syninclusions of fossil nematodes from Miocene Mexican amber (c. 15–20 million years old, see Solórzano Kraemer, 2007 for dating of that amber). Some of these microinclusions that are adhered to nematodes were considered to be stalked adhesive knobs, and some structures inside the nematodes were thought to be zygospores and infesting hyphae. Conidia were also found, and the authors discussed the similarity of the fossils to the modern anamorphic genera Arthrobotrys, Monacrosporium, and Dactylaria. Also, a relationship to the Recent zygomycete genus Stylopage or Cystopage was discussed. However, neither a confident systematic assignment of these fossils nor a safe identification of trapping devices was possible.
Palaeoanellus dimorphus from the Lower Cretaceous of southwestern France is the only Mesozoic evidence of carnivorous fungi so far and the first known fossil fungus that formed hyphal rings as a trapping device. The ring development and the mode of life of P. dimorphus do not conform to that of any modern filamentous predatory fungus. In contrast to the stalked modern trapping rings consisting of three cells, the trapping rings of the fossil are nonstalked, unicellular, and were probably sticky. In the fossil, a yeast stage that occurs for instance in the modern classes Saccharomycetes and Taphrinomycetes is combined with a filamentous ring-forming stage as in modern anamorphs of Ascomycetes. Modern carnivorous Ascomycetes also differ from P. dimorphus because they largely possess septated conidia but also chlamydospores that germinate with hyphae (e.g., Drechsler, 1950). The morphological diversity of the modern species may be very high regarding the diaspores and trapping mechanisms (e.g., Meyer et al., 2005). Regular yeast stages, however, are not known from modern carnivorous fungi. Because of the dimorphic life cycle and the different mode of ring formation, we postulate that Palaeoanellus represents a previously unknown extinct line of carnivorous fungi. The fossil has features of the Hyphomycetes and the Blastomycetes. We assume that the teleomorph of Palaeoanellus belongs to the Ascomycota.
Dimorphism
The different stages of adhered spores show that the primary blastospores formed short acropetal cell chains by polar, subpolar, and rarely lateral formation of budding cells. By further formation of budding cells, these short cell chains finally formed yeast colonies. Budding cells of yeast stages are especially ecologically important in liquid media and were reduced in the course of adaptation of the fungi to terrestrial habitats in favor of filamentous stages. Aquatic representatives of modern carnivorous fungi belong to the same groups as terrestrial soil fungi (see Hao et al., 2005) and are probably secondarily aquatic. In contrast, the dimorphism exhibited by Palaeoanellus dimorphus may represent an early transitional stage from wet to dryer limnetic-terrestrial habitats. Finds of Myrmecia-like green algae and testate amoebae of the genus Centropyxis in the same piece of amber (Girard et al., 2008) strongly support the assumption of a limnetic-terrestrial soil habitat of the fungus.
Carnivory
Nematodes are the most widespread micrometazoans on earth, and they probably developed in coevolution with terrestrial plants (Maggenti, 1981; Poinar et al., 2008). Many fossil taxa resemble modern ones very closely regarding their main diagnostic features. The occurrence of limnetic-terrestrial nematodes already in the Devonian (Poinar et al., 2008) suggests that ecological groups of specialized fungal consumers and decomposers appeared also and diversified very early. It is also likely that, apart from trapping devices of extant carnivorous fungi, different analogous structures were developed by other taxa to occupy this niche. Today, predatory fungi that are specialized in trapping nematodes belong to the most widespread organisms of this ecological group.
Several small nematodes of up to 100 µm in length are located close to a trapping ring of Palaeoanellus dimorphus in the amber (see Schmidt et al., 2007, figs. S1 C, D). Because their maximum diameter falls within the width range of the rings, these animals can be considered as potential prey of the fungus. Other possible prey such as protozoans were also found in the piece of amber. Once trapped, the prey was probably penetrated and digested by infestation hyphae.
Palaeoanellus in the Cretaceous amber forest
As a saprotrophic organism and consumer, the fossil fungus was a part of a highly diverse and complex litter and soil biocenosis of an ancient amber forest. Mixed coastal forests dominated by the conifer families Araucariaceae and Cheirolepidiaceae at the eastern rim of the young Atlantic Ocean were the amber source (Perrichot et al., 2007b). The reconstruction of the depositional environment (Perrichot, 2005; Perrichot et al., 2007a) and the occurrence of marine microorganisms in the amber (Girard et al., 2008) show that these forests grew close to the seashore.
The fungal inclusions originally fossilized in a single piece of amber alongside 79 arthropods and numerous microorganisms such as bacteria, algae, and testate amoebae. Most of these organisms such as schizopterid bugs (Perrichot et al., 2007a) and a mole cricket (Perrichot et al., 2002) are soil and litter-dwelling taxa (for further syninclusions of arthropods, see Perrichot, 2004). This shows that the highly fossiliferous amber piece solidified on the forest floor rather than on the tree bark. Some arthropod inclusions from this deposit are very similar to modern genera, and some microorganisms are even assignable to modern genera. However, Palaeoanellus dimorphus is not the only archaic inclusion in the amber piece. Tiny feathers of a primitive structure, belonging either to an ancestral bird or a nonavian dinosaur, were also fossilized inside (Perrichot et al., 2008).
In the Cretaceous litter and soil biocenosis, Palaeoanellus dimorphus was a specialized consumer of small metazoans and possibly also protozoans. Possessing complex trapping devices to catch motile organisms, it occupied this ecological niche prior to or together with carnivorous fungi of modern lineages. The fossils reveal that already in the Mesozoic some soil fungi were able to increase their nitrogen intake via additional animal food to supplement their diet.
FOOTNOTES
1 The authors thank J. M. Hardesty (Lawrence) and K. Schmidt (Jena) for critical remarks on the manuscript and V. Girard (Rennes), S. Jancke (Berlin), D. Néraudeau (Rennes), and S. Struwe (Berlin) for advice. This work was supported by the German Research Foundation (grant to A.R.S.) and by the Alexander von Humboldt Foundation (grant to V.P.). This study is a contribution to the project AMBRACE (BLAN07-1-184190) of the French National Research Agency. 
6 Author for correspondence (e-mail: alexander.schmidt{at}geo.uni-goettingen.de)
LITERATURE CITED
Ahren, D., AND A. Tunlid. 2003. Evolution of parasitism in nematode-trapping fungi. Journal of Nematology 35: 194–197.[Web of Science][Medline]
Barron, G. L. 1977. The nematode-destroying fungi. Canadian Biological Publications, Guelph, Ontario, Canada.
Barron, G. L. 2003. Predatory fungi, wood decay, and the carbon cycle. Biodiversity 4: 3–9.
Dejax, J., AND E. Masure. 2005. Analyse palynologique de l’argile lignitifère à ambre de l’Albien terminal d’Archingeay (Charente-Maritime, France). Comptes Rendus Palevol 4: 53–65.[CrossRef][Web of Science]
Dove, A. 1987. Räuberische Pilze. Die Neue Brehm-Bücherei, Wittenberg, Germany.
Drechsler, C. 1934. Organs of capture in some fungi preying on nematodes. Mycologia 26: 135–144.[CrossRef]
Drechsler, C. 1950. Several species of Dactylella and Dactylaria that capture free-living nematodes. Mycologia 42: 1–79.[CrossRef][Web of Science]
Girard, V., A. R. Schmidt, S. Struwe, V. Perrichot, G. Breton, AND D. Néraudeau. 2008. Taphonomy and palaeoecology of mid-Cretaceous amber-preserved microorganisms from southwestern France. Geodiversitas 30: in press.
Hao, Y., M. Mo, H. Su, AND K. Zhang. 2005. Ecology of aquatic nematode-trapping Hyphomycetes in southwestern China. Aquatic Microbial Ecology 40: 175–181.[CrossRef][Web of Science]
Jansson, H.-B., AND G. O. Poinar Jr. 1986. Some possible fossil nematophagous fungi. Transactions of the British Mycological Society 87: 471–474.[CrossRef][Web of Science]
Li, S.-D., Z.-Q. Miao, Y.-H. Zhang, AND X.-Z. Liu. 2003. Monacrosporium janus sp. nov., a new nematode-trapping hyphomycete parasitizing sclerotia and hyphae of Sclerotinia sclerotiorum. Mycological Research 107: 888–894.[CrossRef][Web of Science][Medline]
Li, S.-D., K. D. Hyde, R. Jeewon, L. Cai, D. Vijaykrishna, AND K. Zhang. 2005. Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia 97: 1034–1046.
Li, T.-F., K.-Q. Zhang, AND X.-Z. Liu. 2000. Taxonomy of nematophagous fungi. Chinese Scientific and Technological Publications, Beijing, China.
Liou, G. Y., AND S. S. Tzean. 1997. Phylogeny of the genus Arthrobotrys and allied nematode-trapping fungi based on rDNA sequences. Mycologia 89: 876–884.[CrossRef][Web of Science]
Maggenti, A. R. 1981. Nematodes: Development as plant parasites. Annual Review of Microbiology 35: 135–154.[CrossRef][Web of Science][Medline]
Meyer, S. L. F., L. K. Carta, AND S. A. Rehner. 2005. Morphological variability and molecular phylogeny of the nematophagous fungus Monacrosporium drechsleri. Mycologia 97: 405–415.
Néraudeau, D., AND P. Moreau. 1989. Paléoécologie et paléobiogéographie des faunes d’échinides du Cénomanien nord-aquitain (Charente-Maritime, France). Geobios 22: 293–324.[Web of Science]
Néraudeau, D., V. Perrichot, J. Dejax, E. Masure, A. Nel, N. Philippe, P. Moreau, F. Guillocheau, AND T. Guyot. 2002. Un nouveau gisement à ambre insectifère et à végétaux (Albian terminal probable): Archingeay (Charente-Maritime, France). Geobios 35: 233–240.[CrossRef][Web of Science]
Perrichot, V. 2004. Early Cretaceous amber from south-western France: Insight into the Mesozoic litter fauna. Geologica Acta 2: 9–22.
Perrichot, V. 2005. Environnements paraliques à ambre et à végétaux du Crétacé nord-aquitain (Charentes, Sud-Ouest de la France). Mémoires de Géosciences-Rennes 118: 1–310.
Perrichot, V., L. Marion, D. Néraudeau, R. Vullo, AND P. Tafforeau. 2008. The early evolution of feathers: Fossil evidence from Cretaceous amber of France. Proceedings of the Royal Society, B, Biological Sciences 275: 1197–1202.
Perrichot, V., A. Nel, AND D. Néraudeau. 2007a. Schizopterid bugs (Insecta: Heteroptera) in mid-Cretaceous ambers from France and Myanmar (Burma). Palaeontology 50: 1367–1374.[CrossRef][Web of Science]
Perrichot, V., D. Néraudeau, D. Azar, J.-J. Menier, AND A. Nel. 2002. A new genus and species of fossil mole cricket in the Lower Cretaceous amber of Charente-Maritime, SW France (Insecta: Orthoptera: Gryllotalpidae). Cretaceous Research 23: 307–314.[CrossRef][Web of Science]
Perrichot, V., D. Néraudeau, A. Nel, AND G. De Ploëg. 2007b. A reassessment of the Cretaceous amber deposits from France and their palaeontological significance. African Invertebrates 48: 213–227.[Web of Science]
Pfister, D. H. 1997. Castor, Pollux and life histories of fungi. Mycologia 89: 1–23.[CrossRef][Web of Science]
Poinar, G. Jr., H. Kerp, AND H. Hass. 2008. Palaeonema phyticum gen. n., sp. n. (Nematoda, Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 10: 9–14.[Web of Science]
Schmidt, A. R., H. Dörfelt, AND V. Perrichot. 2007. Carnivorous fungi from Cretaceous amber. Science 318: 1743.
Solórzano Kraemer, M. M. 2007. Systematic, palaeoecology, and palaeobiogeography of the insect fauna from the Mexican amber. Palaeontographica Abteilung A 282: 1–133.
Yang, Y., E. Yang, Z. An, AND X. Liu. 2007. Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proceedings of the National Academy of Sciences, USA 104: 8379–8384.
CiteULike Complore Connotea Del.icio.us Digg Facebook Reddit Technorati Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  V. PERRICHOT and V. GIRARD A UNIQUE PIECE OF AMBER AND THE COMPLEXITY OF ANCIENT FOREST ECOSYSTEMS Palaios, March 1, 2009; 24(3): 137 - 139. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
