A new species of Stigmatomyces from Baltic amber, the first

fossil record of Laboulbeniomycetes

Walter ROSSI1*, Marion KOTRBA2 and Dagmar TRIEBEL3

1Department of Environmental Sciences, University of L’Aquila, I-67100 Coppito (AQ), Italy.2Zoologische Staatssammlung Munchen, Munchhausenstraße 21, D-81247 Munchen, Germany.3Botanische Staatssammlung Munchen, Menzinger Straße 67, D-80638 Munchen, Germany.

E-mail : vrossi@univaq.it

Received 5 August 2004; accepted 13 November 2004.

A fossil ascomycete was found attached to the thorax of a stalk eyed fly (Diopsidae : Prosphyracephala succini) in afragment of Baltic amber. The fungus is assigned to the extant genus Stigmatomyces and described as S. succini sp. nov.This find is the first fossil record of the order Laboulbeniales. At the same time it constitutes the oldest record of a

parasitic fungus on an insect. The palaeohabitat is discussed with regard to the find.

INTRODUCTION

Amber is an ancient fossilized resin that frequently haspreserved inclusions of plants, fungi, and animals,among which fungi are relatively rare and insects areparticularly frequent. Most of these inclusions are ofspecies now extinct. They are therefore important forthe understanding of the evolutionary history of extanttaxa.

Baltic and Bitterfeld (Saxon) amber

The most famous amber is the Baltic amber (succinite)which is dates to the Early Eocene and Early Oligocene(ca 35–55 Myr b.p.). It was formed in the vast forests ofFennoscandia, i.e. north of latitude 60x today (Larsson1978, Poinar 1992, Grimaldi 1996). These amber for-ests grew in a warm-temperate to subtropical humidclimate and consisted, apart from conifers, mainly ofArecaceae (palms) and Fagaceae (oaks). The mainresin-producing plants were probably Pinaceae andCupressaceae (Ganzelewski 1997).

These amber trees produced copious amounts ofresin, in which various organisms became entrappedand perfectly preserved. The hardened resin was sub-sequently embedded in the forest floor, and latertransported by floods to the sea. Here the resin becamefossilized during millions of years under high pressure

and anaerobic conditions. The resulting amber wasfinally washed onto the shores of the Baltic Sea, whereit is still found today. Large amounts of this amberwere re-embedded in younger deposits near the seashores in northern Germany. It is generally acceptedthat the amber found near Bitterfeld (Germany) isBaltic amber that was re-deposited in the LowerMiocene (22 Myr b.p.) (e.g. Wunderlich 1983,Weitschat & Wichard 1998, Kutscher 2000, Rikkinenet al. 2003).

Fossil ascomycetes in Tertiary amber

With eleven classes, 56 orders and about 33 000 speciesdescribed up to now, the Ascomycota is the largestphylum in the kingdom Fungi (Kirk et al. 2001,Eriksson et al. 2004). Fossil records are rare. The oldestwell preserved fossil ascomycete with perithecia, asciand ascospores (on stems of a land plant) dates back tothe Early Devonian Rhynie chert, 400 Myr old (Taylor,Hass & Kerp 1997, 1999), which is when the first insectsalso appeared (Upper Devonian: Engel & Grimaldi2004).

Whereas fossil records of Ascomycota are lacking inthe Late Mesozoic, the Tertiary amber deposits of theOld and New World contain a certain number of suchfossils which are well preserved. The oldest deposits inthis formation are those of the Baltic amber (EarlyEocene to Early Oligocene, 35–55 Myr b.p.). Regard-ing the ascomycete fossils of the Baltic amber, there* Corresponding author.

Mycol. Res. 109 (3): 271–274 (March 2005). f The British Mycological Society 271

doi:10.1017/S0953756204001819 Printed in the United Kingdom.

are representatives that could be assigned to fourextant orders : the Capnodiales (with Metacapnodium,Rikkinen et al. 2003), the Graphidales (with Graphis,Garty, Giele & Krumbein 1982), the lichenized Leca-norales (e.g. with Alectoria, Magdefrau 1957, Anzia,Rikkinen & Poinar 2002, Caliciaceae, Rikkinen 2003)and the Mycocaliciales (with a resinicolous species ofChaenothecopsis, Rikkinen & Poinar 2000).

The exact age of the Tertiary Dominican amber is stilla matter of discussion and estimates range from UpperEocene to Miocene (15–45 Myr b.p. ; see Rikkinen& Poinar 2001). The available biostratigraphic andpaleogeographic data, however, clearly indicate anage between 15 and 20 Myr b.p. (Iturralde-Vicente &MacPhee 1996) and therefore Dominican amber is lessthan half the age of Baltic amber. The fossilizedAscomycota found until now in the Dominican depositsbelong to four orders and are assigned to extant gen-era: the Clavicipitales (with the anamorphic genusBeauveria on a worker ant, Poinar & Thomas 1984),the Eurotiales (with Aspergillus, Thomas & Poinar1988), the Lecanorales (with Parmelia Poinar, Peterson& Platt 2000) and the Xylariales (with Xylaria, Poinar& Poinar 1999).

Summarizing all of these records, there are onlyseven of the 56 orders belonging to four of the elevenclasses of the Ascomycota documented in Tertiary am-ber (the Sordariomycetes, Eurotiomycetes, Dothideo-mycetes, and Lecanoromycetes). With Stigmatomycessuccini described below, the first representative of theorder Laboulbeniales (class Laboulbeniomycetes) canalso be added.

Fossil fungi associated with insects

As far as we know, there exists no fossil record of fungiassociated with insects prior to the Tertiary. The hy-phomycete Sporotrichites heterospermus reported byGoeppert & Berendt (1845) from a fly in Baltic ambermight be the first and possibly oldest record of such anassociation. The fungus, however, might be regarded assaprophytic (Poinar & Thomas 1982).

Majewski (1994) reported finding Laboulbenialesthalli on the abdomen of a staphylinid beetle fromBaltic amber, but later corrected his statement as thesewere actually large and peculiarly shaped setae of thebeetle (Majewski, in litt.).

Two fungi presumably living as more or less host-specific parasites on insects were found in Dominicanamber : a representative of the genus Beauveria (ana-morphic Clavicipitales) on a worker ant (Poinar &Thomas 1984) and a zygomycetous fungus of the genusEntomophthora (Entomophthorales) invading a termite(Poinar & Thomas 1982).

As Dominican amber is considerably younger thanBaltic amber (see above), Stigmatomyces succini fromthe Bitterfeld amber is the oldest record of a fungusregarded as a host-specific parasite of an insect.

Laboulbeniales and Diopsidae

Laboulbeniales are obligate ectoparasites of arthro-pods, especially insects. They are peculiar in lacking atypical hyphal system, which is replaced by a minutecompact thallus. About 2000 species of Laboulbenialeshave been described so far, about 200 of which occuron flies (for a SSU rDNA phylogeny of Laboulbenialessee Weir & Blackwell 2001). Laboulbeniales parasitic onDiptera are frequently clubshaped, although some havelong appendages, so they look like a tiny tree attachedto the host cuticle. 21 Laboulbeniales have been de-scribed from members of the dipteran family Diopsidae(stalk-eyed flies). These fungi are distributed in threegenera: Laboulbenia (3 species), Rhizomyces (9) andStigmatomyces (9) (Thaxter 1896, 1908, 1931, Rossi1982, 1987, 1990). Some Laboulbeniales exhibit a highdegree of host specificity and according to Feijen (1989)the study of parallel evolution between Diopsidae andtheir Laboulbeniales promises to be a rewarding topic.

The most basal lineage of the Diopsidae is the extinctspecies Prosphyracephala succini, which is known fromBaltic amber (Loew 1873, Meunier 1903, Schumann1994).

During a recent study of Prospyracephala, a tuft ofLaboulbeniales, however, was discovered on the thoraxof one specimen; this gave rise to the present investi-gation.

MATERIALS AND METHODS

The amber fragment studied measures 12.3r9.9r4.8 mm. It is polished with one plane and oneirregular face, and four narrow facets along the sides.In addition to the Prosphyracephala succini specimenwhich bears the Laboulbeniales, one male Elephan-tomyia brevipalpa Loew 1851, three male phorids andanother badly damaged phorid are embedded in thechunk, as well as a few stellate hairs, typical for Balticamber. The specimen was purchased from a privateamber collector, Manfred Kutscher (Sassnitz, Ger-many), who had discovered it in material from theBitterfeld deposit. Microscopic examination and pho-tography were performed with a Leica MZ 12 stereo-scope equipped with Carl Zeiss AxioCam HR digitalcamera and AxioVision 3.0.6. SP4 software.

TAXONOMY

Stigmatomyces succini W. Rossi, Kotrba & Triebel,sp. nov. (Figs 1–2)

Fungus fere directus, perithecii collo extra curvato, appendice

divaricata. Basalis ac suprabasalis cellulae longitudine sub-aequae. Cellula stirpis perithecii exilis ac elongata. Duaesuperiores appendicis cellulae magnae, quarum ultima duo

diducta antheridia incurvato ac elongato collo fert, penultimavero antheridium unum. Appendicis basalis cellula prob-abiliter sterilis. Perithecii basales cellulae una cum cellula

stirpis elongatum corpum efficientes. Perithecii venter cumsuis basalibus cellulis fere ellipticum, circiter triplo ac dimidio

The first fossil Laboulbeniomycete 272

longius quam latius, a collo parum distinctum. Peritheciicollum comparate breve, inferiore parte crassa ac decrescenti,

superiore vero angusta ac elongata, dilatato apice.Typus : Germany : Bitterfeld deposit, parasitus Prosphyra-

cephalae succini in succino servatae,M.Kutscher (ZoologischeStaatssammlung Munchen – holotypus).

Thalli about 0.3 mm long, nearly straight, the neckslightly curved outward, the appendage divergent andcurved upward. Receptacle slender. Basal and supra-basal cells almost equal in length. Stalk cell of theappendage slender and elongate, the two upper cells ofthe appendage large and stout, the terminal one bearingtwo antheridia whose necks are slightly curved, diver-gent and unusually long, while the subterminal onebears a single antheridium. The presence of a sterilebasal cell is supposed, but cannot be clearly seen. Septadividing stalk and basal cells of perithecium not visible,but these cells form a relatively elongate region, abovewhich the perithecial venter is distinguished only by aslight elevation. Perithecial venter, together with thecells below it, almost elliptical, about three and a halftimes longer than broad, distinguished by a slightelevation from the large base of the neck; the latter

relatively short, with a stout, slightly tapering lowerportion and with an upper portion narrow and elon-gate; the tip slightly enlarged, but details of the lips arenot visible.

The amber fragment is deposited in the Diptera col-lection of the Zoologische Staatssammlung Munchen.The new species is represented by four thalli, three ofwhich are mature and complete, positioned on theright anterior portion of the scutum of a specimen ofProsphyracephala succini (Diptera : Diopsidae).

Stigmatomyces succini differs from the known extantspecies of Stigmatomyces in the very low number ofantheridia and, above all, the elongation of the efferenttube of the same. It further differs from the otherStigmatomyces species parasitic on Diopsidae in theshort perithecial neck.

DISCUSSION

It is not easy to suggest any relationship of the newfossil species Stigmatomyces succini with the extantspecies of the genus. The fossil species is not very

Figs 1–2. Stigmatomyces succini (holotype). Fig. 1. Stalk-eyed fly Prosphyracephala succini with a tuft of S. succinithalli attached to the thorax (arrow). Fig. 2. S. succini thalli at higher magnification. Bar=100 mm.

W. Rossi, M. Kotrba and D. Triebel 273

different from the other Stigmatomyces species para-sitic on Diopsidae (e.g. S. gregarius) as to the generalhabit. However, among the latter S. beccarii, parasiticon Sphyracephala beccarii from Malawi, is the onewith the lowest number of antheridia and the shortestperithecial neck, and thus the most similar to S. succini.Although Prosphyracephala succini is not more closelyrelated to Sphyracephala beccarii than to any otherDiopsinae, the two host taxa are still the most similarmorphologically due to plesiomorphies, and possiblyalso with respect to their life history.

According to Feijen (1989), the gregarious habits,adult longevity and life in wet biotopes are pre-requisites for host receptivity for Laboulbeniales.P. succini likely dwelled in a high humidity environ-ment in the vicinity of freshwater, e.g. on the vegetationnear a forest stream or directly on the river banks, as domost of the extant Sphyracephalinae. Like many recentDiopsidae, the flies may have lived in dense aggre-gations with particularly high mating activity duringpart of the year, which would facilitate transmission ofthe fungus infection among conspecifics.

ACKNOWLEDGEMENTS

We thank Manfred Kutscher (Sassnitz) for providing the amber

specimen and Helmut Mayr (Palaontologische Staatssammlung

Munchen) for help with rare literature. Thanks are also due to David

Grimaldi American Museum of Natural History (New York) for

useful comments on the paper.

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