Beetle borings in wood with host response in early Permian conifers from Germany
Wood boring represents a common feeding and survival strategy in several lineages of beetles. The larvae of wood-boring beetles hatch and excavate tunnels in wood during their development. The origin and evolutionary history of this life habit, however, remain poorly understood to date, as the fossil record is scarce. We present new silicified conifer wood specimens containing complex borings from the lowermost Permian Manebach Formation of the Thuringian Forest Basin in central Germany and the lower Permian Donnersberg Formation of the Saar–Nahe Basin in southwestern Germany. Additionally, this distinctive type of wood boring is recorded from the Carboniferous/Permian of the Czech Republic, Poland and China. For these borings, the new fodinichnion or agrichnion Pectichnus multicylindricus igen. et isp. nov. is established. It is characterised by several parallel cylindrical tunnels in a longitudinal arrangement, branching from a tangential primary tunnel oriented perpendicularly. The borings contain frass as coprolites made up of undigested wood cells. The conifer trees responded to the borings with callus production that subsequently filled or enclosed the tunnels. This is the earliest record of this specific life habit of ancient insects. The novel wood-boring strategy required structural modification and physiological adaptation; it probably emerged when insect diversity expanded considerably as terrestrial environments changed dramatically.
KeywordsWood boring Coleoptera Conifers Wound response Bioerosion Permian
Wood boring is a specific life habit that occurs in several extant groups of terrestrial arthropods, among them detritivorous oribatid mites and numerous insect families (e.g., Vité 1952; Hickin 1963; Solomon 1995; Kellogg and Taylor 2004; and references therein). In modern terrestrial ecosystems, several major and many minor lineages of coleopterans (beetles) are one of the predominant groups amongst arthropod wood borers (e.g., Johnson and Lyon 1991; Solomon 1995; Krantz and Walter 2009). Comparisons with modern representatives indicate that most of the Paleozoic wood borings were produced by oribatid mites, which can be traced back to the Devonian (Labandeira et al. 1997). Although borings in the Late Carboniferous cordaitean root Premnoxylon from Lewis Creek of the United States have been considered to be produced by ancestral beetles (Cichan and Taylor 1982; Scott and Taylor 1983), the small (up to 75 μm long) ellipsoidal coprolites contained in the borings appear to be too small for all known beetle families.
To date, the earliest known beetle wood borings were documented in middle Permian conifer wood from Tikhie Gory, Russia (Naugolnykh and Ponomarenko 2010). From the late Permian, beetle wood borings have been reported from glossopterid tree axes of South Africa (Zavada and Mentis 1992) and conifer wood from Antarctica (Weaver et al. 1997). Some complex wood borings attributed to polyphagous beetles have recently been recognised in conifer wood from North China (Feng et al. 2017). They demonstrate complex dietary changes during the development of the beetle larvae and provide a unique glimpse into the early evolution of insect farmers and subsociality.
In this contribution, we describe new fossil material from the lower Permian of Germany showing similar structures to the North China wood borings. The findings not only represent the oldest evidence of wood-boring beetles but also shed new light on the evolution of insect life habits and the plant–beetle co-evolutionary history.
Geology, materials and methods
The fossil site Crock is situated ca. 10 km southeast of Schleusingen, in the South of Thuringia (Feng et al. 2015). Historically, there were several coal mines producing anthracite coal from the lower Permian of Crock. Crock is the only known locality within the Thuringian Forest Basin yielding lower-ranked coals that proved useable for cuticle maceration (Kerp and Barthel 1993). Although there is a long history of both fossil collecting and palaeobotanical research in the Thuringian Forest Basin (Barthel 2003, 2004, 2005, 2006, 2007, 2008), fossil wood has been reported only occasionally (Barthel et al. 2010). Several new types of fossil wood have recently been described in detail from Crock (Witter et al. 2011), including a specialised feeding trace of oribatid mites preserved in a conifer wood (Feng et al. 2015).
The specimen described from Crock was found in coarse-grained alluvial fan deposits exposed on the slopes of the Irmelsberg Hill. These sediments from the southwestern part of the so-called Schleusingen marginal zone belong to the southernmost occurrence of the Rotliegend Group, consisting of lower to middle Permian (Cisuralian) strata of the Thuringian Forest Basin. These wood-containing basal alluvial fan deposits are overlain by coal-bearing, fine-grained clastic sequences, which have been assigned to the Manebach Formation (Lützner et al. 2012). The stratigraphic level of the fossil wood locality in the basal Rotliegend strata is early Asselian.
Fossil wood from the Winnweiler site has been attracting scientific attention since the previous century (e.g., Schuster 1908). This may be due to the fact that large numbers of fossil wood specimens are being exposed on the surface. The exact stratigraphic origin of the wood-bearing horizon remained uncertain for a long time, although the plant assemblage represents an early Permian xeromorphic upland vegetation, which is predominated by diverse cordaitaleans and conifers due to the impression and petrified wood fossils (Gothan 1905; Noll et al. 2005; Noll 2012).
Petrified wood from Winnweiler is parautochthonously embedded in volcaniclastic deposits of the Wingertsweilerhof Subformation, belonging to the middle to upper portion of the Donnersberg Formation (Lorenz and Haneke 2004). This subformation is characterised by alluvial fans, and braided and meandering river deposits, including associated floodplains, within the half-graben of the Saar–Nahe Basin (Haneke et al. 2012). The Donnersberg Formation comprises voluminous subvolcanic, effusive, pyroclastic and epiclastic rocks, representing persistent synsedimentary volcanism during the Artinskian (Lorenz and Haneke 2004). The Winnweiler sediments are derived from the Donnersberg eruptive centre 6 km to the northeast, and consist of stacked debrites representing repeated deposition by mass flows and hyperconcentrated flows within ephemeral channels. Silicified wood of varying size, fragmentation and preservation occurs at the top of the non-stratified debrites roughly or not aligned (Trümper et al. 2018). Medium- to small-scale cross-bedded sandstones and siltstones at the top of the channel fills contain plant fossils as imprints and indicate gradually, but rapidly declining sediment contents and flow velocities following the mass flows.
The majority of secondary xylem fragments investigated from Winnweiler are of the pycnoxylic type, which is best referred to the genus Agathoxylon Hartig (Rößler et al. 2014). However, some specimens with sclerenchyma nests in the pith can be assigned to the Tylodendron-type conifers (Noll and Wilde 2002). All of the wood samples including thick woody trunks, side branches and roots in this locality commonly exhibit distinct growth rings that resulted from regular climatic fluctuations. The growth rings show notable ring boundaries and a small amount of latewood. This type of growth ring coincides with the type 1 growth rings in the contemporaneous Chemnitz fossil lagerstätte (Luthardt et al. 2017), and thus probably corresponds to the regular sunspot activities during the early Permian (Luthardt and Rößler 2017).
The bored wood collected at Crock and Winnweiler was ground and polished for detailed examination. Photographs were produced with a Nikon Eclipse ME600 transmitted light microscope and a Nikon SMZ1500 stereoscopic light microscope. Images were taken on both microscopes, which were equipped with a Nikon DS-5M-L1 digital camera. Composite images were stitched using Adobe® Photoshop® CS5 Extended program software. The specimens are stored at the Museum für Naturkunde Chemnitz (MfNC), Germany, labelled as K6674, K6675, K6676 and K6677 for Winnweiler specimens, and K6678 for the Crock specimen.
Ichnofamilia Talpinidae Wisshak, Knaust et Bertling, 2019
Ichnogenus Pectichnus nov.
Type ichnospecies Pectichnus multicylindricus. igen. et isp. nov.
Etymology. Latinised after the Classic Greek pektos = combed and ichnos = trace.
Diagnosis. Single horizontal tangential gallery in bark/wood, secondarily branching off in longitudinal tunnels at right angles corresponding to the host axis.
Pectichnus multicylindricus isp. nov.
Etymology. Latin multus = many; cylindrus = cylinder.
Diagnosis. Pectichnus with equally-spaced, parallel secondary cylindrical tunnels gradually merging into the secondary xylem and longitudinally extending from the main gallery at the interface of bark and secondary xylem.
Locality and horizon. Winnweiler, Rhine-Palatinate State, southwestern Germany; Donnersberg Formation, Rotliegend, Asselian, early Permian.
Description. The specimens from the Shitanjing Coalfield, Ningxia Huizu Autonomous Region, Northwest China, consist of axes of the conifer Ningxiaites specialis Feng 2012. They are permineralised by silica and were found in the Sunjiagou Formation of Changhsingian, late Permian, age. The beetle–plant interactions, including distinctive galleries and tunnels inside the tree tissues, have been described in detail by Feng et al. (2017). Five sequential phases in the life cycle of wood-boring beetles were recognised by the authors. Two series of borings, one comprising 11 subsidiary cylindrical tunnels (and an associated triangular callus), another showing lateral borings embedded in wood (Fig. 2a).
The conspicuous wood-boring pattern was also recognised in two Late Carboniferous or early Permian specimens in the collection Niemirowska. No. 264 from Poland shows borings with 11 subsidiary tunnels (Fig. 2b); No. 2992 from the Czech Republic (Fig. 2c) shows borings with eight subsidiary tunnels. Wound reaction tissue in both specimens indicates that the host trees were alive. It has filled in the tunnels but, nevertheless, preserved their shape. This response does not constitute a part of the diagnosis, as embedment structures are not trace fossils (Bertling et al. 2006).
Both the longitudinal and tangential borings are infilled with large coprolites (Fig. 4a–c, f). They are spheroidal to indistinctly shaped with diameters varying from 0.2 to 1.1 mm (av. 0.5 mm, n = 55). The coprolites are formed by masses of undigested plant tissues (Fig. 4g, h). In some cases, fragments of tracheids and rays can be recognised in the coprolite matrix. Some tangential borings show wound reaction with contorted wood tissue (Fig. 4i, arrow).
A complete boring series possessing six parallel tunnels is well preserved in one specimen (Fig. 5a), while the borings in the other specimens are incompletely preserved (Fig. 5b–d). Structurally, the Winnweiler borings are identical to the longitudinal borings from Crock, which run in one single growth ring. The cylindrical tunnels are (sub)circular in cross-section and have an average diameter of 5 (3.5–6.5) mm. A longitudinal section shows that the tunnel is up to 40 mm long.
Remarks. The early Permian borings from central and southwestern Germany are arranged in parallel series of up to 11 longitudinal tunnels; tangential tunnels are rarely seen. Due to the incompleteness of the specimens, the connection of both tunnel orientations remains somewhat obscure, although they occur very close to each other and possess similar diameters.
The brief review of bioerosion ichnotaxa by Wisshak et al. (2019) reveals that no similar structures have yet been described, let alone named. The ichnotaxonomical treatment of wood borings is yet in its infancy, and we encourage subsequent authors to formally describe their finds, following the path set by Wisshak et al. (2019) and respecting the rules of the International Code of Zoological Nomenclature (1999) and the widely accepted guidelines of Bertling et al. (2006).
Known stratigraphic and palaeogeographic distribution. Carboniferous–Permian of Europe (Germany, Poland and Czech Republic) and Asia (China).
The German borings frequently contain large coprolites and are distributed in the secondary xylem of the host conifers. Even if evidence of body fossils is lacking in this material, the position, tunnel geometry and coprolite dimension suggest that beetles produced these borings (see e.g. Vité 1952; Gullan and Cranston 2014). The material from the upper Permian of North China is better preserved, and it comprises body fragments of the producers (Feng et al. 2017), so the interpretation of the authors is followed here. The boring system appears to have been produced by an adult female beetle laying eggs in a tangential tunnel between wood and bark and by growing larvae feeding in longitudinal subsidiary tunnels inside the wood.
Probable beetle borings have been documented in fungus-infected conifer-like wood from the lower Kazanian, middle Permian, of Tatarstan, Russia (Naugolnykh and Ponomarenko 2010). They are principally oriented longitudinally, parallel to the wood axis, and are connected by short shafts of varying orientation. The authors suggest Permocupedidae as the most likely producers, but their material differs strongly from the one presented here. The adult body shape of this family seems to preclude that its members have produced Pectichnus (Feng et al. 2017). This points to the Tshekardocoleidae as potential tracemakers, as this is the only other beetle family known from the lower Permian (Ponomarenko 2003). The body fossil record is very likely incomplete, however, so that other, yet unknown, insects may be the producers.
The position, geometry, extent and sequence of borings within host plants reflect the consumption strategy of a wood-boring beetle (Gullan and Cranston 2014). Our material provides strong evidence for the consumption of different plant tissues during the beetles’ ontogeny. Serial sections indicate that the longitudinal tunnels commenced close to the cambial layer of the conifer tree, but subsequently completely emerged into the secondary xylem, suggesting that the larvae may have consumed mainly wood tissues.
Tunneling wood represents a complex life strategy of insects, which effectively avoid predation and fungal parasites for their offspring (Raffa et al. 2015). Contrary to Nel et al. (2018), who claim that significant changes in mouthpart morphologies of insects cannot been recognised during the Late Carboniferous to middle Permian, the wood borings reported here imply a series of functional innovation, especially regarding mouthparts and cellulose digestion. Compared with other vegetative organs, wood is a relatively nutrition-poor food source. For this reason, approximately 10% of all extant insect wood borers accommodate intracellular endosymbionts in their gut cells or gut lumen (Schoonhoven et al. 2006). Cellulose-digesting microorganisms as gut symbionts not only help to digest cellulose but also enhance the nutritional quality of wood (Schowalter 2017). Gut mixing is especially important for digestion of cellulose and lignin into labile carbohydrates and concentration of nitrogen and other nutrients (Breznak and Brune 1994), which may fuel nitrogen fixation by microbes in xylophage guts (Nardi et al. 2002).
Among extant wood-boring insects, ectosymbioses are widespread as associations with microscopic fungi (e.g., Six 2012; Meurant 2017). These fungi degrade woody debris lodged in tunnels or the wood itself, thus providing the important service of cellulose degradation for the wood borers (Haack and Slansky 1987; Hernández-García et al. 2017; Birkemoe et al. 2018). Fossil evidence for the presence of cellulolytic fungi in wood borings demonstrates that obligate nutritional dependency on fungi of wood-boring beetles occurred already during the late Permian (Feng et al. 2017). The occurrence of fungal hyphae within borings suggests that those beetle occupants were probably early farmers, resembling modern bark beetles, macrotermitine termites and attine ants (Farrell et al. 2001; Biedermann et al. 2009; Wilson and Nowak 2014). Features of fungal decay, however, have not been observed in the European Permian wood borings. This suggests that their producers possessed intestinal microbiomes for the digestion process rather than being mycophagous. In this context, it is worth noting that wood decay structures were not observed in the early Permian oribatid mite borings from the Crock locality (Feng et al. 2015). The reason may be that fungal ectosymbionts had not been functionally adopted by the terrestrial arthropods during the early Permian.
On the other hand, it is hard to imagine that a beetle with mycophagous larvae (late Permian of China) should produce the same type of borings as a xylophagous representative (early Permian of Europe). In due course, the ichno-ethological classification remains somewhat uncertain: given the volumetrical dominance of larval longitudinal tunnels with coprolites containing wood fragments, Pectichnus has largely to be regarded as a fodinichnion, although the tangential gallery bored by the mother beetle has calichnial quality. If the hyphae in the late Permian Chinese samples prove to be relics of ambrosia-type fungi, however, this would qualify the borings as agrichnia.
The parallel path of the tunnels described here is direct evidence for thigmotaxis of the beetle borers already developed in the earliest Permian. Larvae of extant bark beetles (Scolytidae) similarly avoid contact when jointly tunneling the wood substrates (Beaver 1974). Keeping the tunnels at a distance precludes intraspecific (conspecific) competition in the larval stages, thus effectively reducing the mortality of the population (De Jong and Grijpma 1986; Byers 1989; Kirkendall 1989; Legros et al. 2009).
Crowson (1975) and Ponomarenko (2003) associate the origin of beetles with the breakdown of wood. Understanding the autecology of the Pectichnus producers therefore has implications not only for the assessment of biotic interactions in Permian terrestrial ecosystems but also for the co-evolutionary history of the associated organisms (cf. Labandeira 2013). Two conifer species are identified as host plants for the wood borers under discussion, indicating that the wood-boring habit developed as a rather broad trait. Given the wood and bark structures available as substrates for Late Paleozoic borers, it does not come as a surprise (a) to see conifer wood as the prime target of their attack, and (b) to register very few (if any) pre-Permian insect borings (Scott et al. 1992). On the other hand, the tunnel-enclosing sequence by reaction-wood circumvallation shows that the ancient conifers were well primed for the beetle’s attack. It should be noted that the formation of an epicormic shoot in the traumatic area indicates an advanced physiological feature as wound response of the host plants (Decombeix et al. 2010, 2018), which is similar to modern conifers (Krokene 2015).
The diversity of herbivorous insects displays a dramatic expansion during the Late Carboniferous (Scott et al. 1992; Labandeira and Currano 2013), in accordance with a series of significant geological events at that time (Montañez et al. 2016). The coprolites contained in wood borings in Carboniferous cordaitalean wood have previously been claimed as produced by ancestral beetles (Scott and Taylor 1983). Large coprolites and millipede larva, however, have been observed in the central pith cavity of the largest Permian calamite (Arthropitys bistriata) trunk from the Chemnitz fossil lagerstätte (Rößler et al. 2012). This indicates that wood-boring habits originated in a parallel and perhaps penecontemporaneous manner in various arthropod groups; it could plausibly be extended into the Carboniferous. For the time being, the earliest definitive beetle body fossils are early Permian in age (Ponomarenko 1963; Kukalová-Peck and Beutel 2012; Toussaint et al. 2017). In addition, probable beetle coprolites have been widely documented in a variety of Permian host plants (Weaver et al. 1997; D’Rozario et al. 2011), indicating a previous existence for some stem-group lineages of the Coleoptera (McKenna et al. 2015).
The sudden rise of insect diversity lead to interspecific competition for habitat niches and food sources; it may have resulted in stressful ecological conditions for the individual populations (Labandeira and Currano 2013; Nicholson et al. 2014; Dmitriev et al. 2018). Therefore, we propose that the wood-boring habit of beetles could have emerged under the combined pressure of insect expansion and dramatic environmental changes. The form of the boring system described herein and the behaviour indicated by it suggests that one of the earliest lineages of the Polyphaga, one of the four main beetle clades, was probably present prior to the Carboniferous–Permian transition.
Detailed analysis of wood borings from two early Permian conifer hosts provides the earliest direct evidence of secondary xylem utilisation by beetles. The novel feeding behaviour implied functional innovation in digestive adaptation. The boring pattern is highly distinctive and ichnotaxonomically established herein as Pectichnus multicylindricus igen. et isp. nov. Its stratigraphic and palaeogeographic distribution is enlarged considerably. As the host plants were still alive at the time of the beetle attack, they responded by subsequent fill and circumvallation of the borings as a wound reaction. This shows that physiological responses to borings were well established already at the beginning of the co-evolutionary history of wood-boring beetles and conifer trees.
We dedicate this paper to Professor Dr Hans Kerp on the occasion of his 65th birthday in 2019 and express our sincere gratitude for his generous help and stimulating interest. The authors deeply appreciate the invitation of the guest editors of this special volume, Benjamin Bomfleur, Michael Krings and Christian Pott. Steffen Trümper kindly provided geological information about the fossil site Winnweiler, and Ludwig Luthardt investigated tree ring characteristics. We thank Mathias Merbitz and Hubert Bieser for technical support in preparation work, Jorge Genise, Sebastian Voigt and an anonymous reviewer for the constructive comments on the paper, and Mrs Sandra Niemirowska for providing photographs and the generous access to her private collection. This study was jointly supported by the National Natural Science Foundation of China (U1702242, 41672015), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB26000000), the Yunnan Provincial Science and Technology Department (2019JIEQING01), the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (20161101), the China Geological Survey (DD20190022) and the Deutsche Forschungsgemeinschaft (DFG grant RO 1273/4-1 to RR).
- Barthel, M. 2003. Die Rotliegendflora des Thüringer Waldes. Teil 1. Veröffentlichungen Naturhistorisches Museum Schleusingen 18: 3–16. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M. 2004. Die Rotliegendflora des Thüringer Waldes. Teil 2. Veröffentlichungen Naturhistorisches Museum Schleusingen 19: 19–48. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M. 2005. Die Rotliegendflora des Thüringer Waldes. Teil 3. Veröffentlichungen Naturhistorisches Museum Schleusingen 20: 27–56. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M. 2006. Die Rotliegendflora des Thüringer Waldes. Teil 4. Veröffentlichungen Naturhistorisches Museum Schleusingen 21: 33–72. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M. 2007. Die Rotliegendflora des Thüringer Waldes. Teil 5. Veröffentlichungen Naturhistorisches Museum Schleusingen 22: 41–67. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M. 2008. Die Rotliegendflora des Thüringer Waldes. Teil 6. Veröffentlichungen Naturhistorisches Museum Schleusingen 23: 39–62. (= Teil 1–6 see Sonderveröffentlichung, Veröffentlichungen Naturhistorisches Museum Schleusingen, 2009).Google Scholar
- Barthel, M., M. Krings, and R. Rößler. 2010. Die schwarzen Psaronien von Manebach, ihre Epiphyten, Parasiten und Pilze. Semana 25: 41–60.Google Scholar
- Crowson, R.A. 1975. The evolutionary history of Coleoptera, as documented by fossil and comparative evidence. Atti X Congresso Nazionale Italiano di Entomologia 10: 7–90.Google Scholar
- Dmitriev, V.Yu., D.S. Aristov, A.S. Bashkuev, D.V. Vasilenko, P. Vřsanský, A.V. Gorochov, E.D. Lukashevitch, M.B. Mostovski, A.G. Ponomarenko, YuA Popov, A.P. Rasnitsyn, N.D. Sinitshenkova, I.D. Sukatsheva, M.M. Tarasenkova, A.V. Khramov, and A.S. Shmakov. 2018. Insect diversity from the Carboniferous to recent. Paleontological Journal 52(6): 610–619.CrossRefGoogle Scholar
- D’Rozario, A., C. Labandeira, W.-Y. Guo, Y.-F. Yao, and C.-S. Li. 2011. Spatiotemporal extension of the Euramerican Psaronius component community to the Late Permian of Cathaysia: In situ coprolites in a P. housuoensis stem from Yunnan Province, southwest China. Palaeogeography, Palaeoclimatology, Palaeoecology 306: 127–133.CrossRefGoogle Scholar
- Gothan, W. 1905. Zur Anatomie lebender und fossiler Gymnospermenhölzer. Abhandlungen der Königlich-Preußischen Geologischen Landesanstalt 44: 1–108.Google Scholar
- Gullan, P.J., and P.S. Cranston. 2014. The insects: an outline of entomology, 5th ed. Chichester: Wiley-Blackwell.Google Scholar
- Haack, R., and F. Slansky. 1987. Nutritional ecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. In Nutritional ecology of insects, mites, spiders, and related invertebrates, ed. F. Slansky, 449–486. New York: Wiley.Google Scholar
- Haneke, J., V. Lorenz, and H. Stollhofen. 2012. Donnersberg-Formation. In Stratigraphie von Deutschland X. Rotliegend. Teil I: Innervariscische Becken, eds. H. Lützner, and G. Kowalczyk. Schriftenreihe der Deutschen Gesellschaft für Geowissenschaften 61: 254–377.Google Scholar
- Hickin, N.E. 1963. The insect factor in wood decay. London: Associated Business Programmes.Google Scholar
- ICZN [International Commission on Zoological Nomenclature]. 1999. International Code of Zoological Nomenclature, adopted by the International Union of Biological Science, 4th ed. London: International Trust for Zoological Nomenclature.Google Scholar
- Johnson, W.T., and H.H. Lyon. 1991. Insects that feed on trees and shrubs, 2nd ed. New York: Cornell University Press.Google Scholar
- Krantz, G.W., and D.E. Walter. 2009. A manual of acarology, 3rd ed. Lubbock: Texas Tech University Press.Google Scholar
- Krokene, P. 2015. Conifer defense and resistance to bark beetles. In Bark beetles: biology and ecology of native and invasive species, eds. F.E. Vega and R.W. Hofstetter, 1–40. Amsterdam: Elsevier.Google Scholar
- Lorenz, V., and J. Haneke. 2004. Relationship between diatremes, dykes, sills, laccoliths, intrusive-extrusive domes, lava flows, and tephra deposits with unconsolidated water-saturated sediments in the late Variscan intermontane Saar–Nahe Basin, SW Germany. In Physical geology of high-level magmatic systems, eds. C. Breitkreuz and N. Petford, 75–124. London: The Geological Society of London (= Geological Society of London, Special Publications 234).Google Scholar
- Lützner, H., D. Andreas, J.W. Schneider, S. Voigt, and R. Werneburg. 2012. Stefan und Rotliegend im Thüringer Wald und seiner Umgebung. In Stratigraphie von Deutschland X. Rotliegend. Teil I: Innervariscische Becken, eds. H. Lützner, and G. Kowalczyk. Schriftenreihe der Deutschen Gesellschaft für Geowissenschaften 61: 418–487.Google Scholar
- McKenna, D.D., A.L. Wild, K. Kanda, C.L. Bellamy, R.G. Beutel, M.S. Caterino, C.W. Farnum, D.C. Hawks, M.A. Ivie, M.L. Jameson, R.A.B. Leschen, A.E. Marvaldi, J.V. Mchugh, A.F. Newton, J.A. Robertson, M.K. Thayer, M.F. Whiting, J.F. Lawrence, A. Ślipiński, D.R. Maddison, and B.D. Farrell. 2015. The beetle tree of life reveals that Coleoptera survived end-Permian mass extinction to diversify during the Cretaceous terrestrial revolution. Systematic Entomology 40(4): 835–880.CrossRefGoogle Scholar
- Meurant, G. 2017. Insect–fungus interactions, 14th ed. London: The Royal Entomological Society of Society of London.Google Scholar
- Noll, R. 2012. Anatomische Beobachtungen am Sekundärxylem permischer Koniferen- und Cordaitenhölzer der Donnersberg-Formation. Veröffentlichungen des Museums für Naturkunde Chemnitz 35: 29–38.Google Scholar
- Noll, R., and V. Wilde. 2002. Conifers from the “Uplands”—Petrified wood from Central Germany. In Secrets of petrified plants—fascination from millions of years, eds. U. Dernbach and W.D. Tidwell, 88–103. Heppenheim: D’ORO.Google Scholar
- Noll, R., R. Rößler, and V. Wilde. 2005. 150 Jahre Dadoxylon—Zur Anatomie fossiler Koniferen- und Cordaitenhölzer aus dem Rotliegend des euramerischen Florengebietes. Veröffentlichungen des Museums für Naturkunde Chemnitz 28: 29–48.Google Scholar
- Ponomarenko, A.G. 1963. Paleozoyskie zhuki Cupididea evropeyskoy chasti SSSR. Paleontologicheskii Zhurnal 1963(1): 70–85.Google Scholar
- Ponomarenko, A.G. 2003. Ecological evolution of beetles (Insecta: Coleoptera). Fossil Insects. Acta Zoologica Cracoviensia 46(supplement): 319–328.Google Scholar
- Raffa, K.F., J.-C. Grégoire, and B.S. Lindgren. 2015. Natural history and ecology of bark beetles. In Bark beetles: biology and ecology of native and invasive species, eds. F.E. Vega and R.W. Hofstetter, 1–40. Amsterdam: Elsevier.Google Scholar
- Rößler, R., M. Philippe, J.H.A. van Konijnenburg-van Cittert, S. McLoughlin, J. Sakala, G. Zijlstra, M. Bamford, M. Booi, M. Brea, A. Crisafulli, A.-L. Decombeix, M. Dolezych, T. Dutra, L.G. Esteban, P. Falaschi, Z. Feng, S. Gnaedinger, M.G. Sommer, M. Harland, R. Herbst, E. Iamandei, S. Iamandei, H. Jiang, L. Kunzmann, F. Kurzawe, S. Merlotti, S. Naugolnykh, H. Nishida, R. Noll, C. Oh, O. Orlova, P. de Palacios, I. Poole, R.R. Pujana, A. Rajanikanth, P. Ryberg, K. Terada, F. Thévenard, T. Torres, E. Vera, W. Zhang, and S. Zheng. 2014. Which name(s) should be used for Araucaria-like fossil wood? Results of a poll. Taxon 63(1): 177–184.CrossRefGoogle Scholar
- Schoonhoven, L.M., J.J.A. Van Loon, and M. Dicke. 2006. Insect–plant biology. Oxford: Oxford University Press.Google Scholar
- Schowalter, T.D. 2017. Insect ecology, an ecosystem approach, 4th ed. Baton Rouge: Elsevier.Google Scholar
- Schuster, J. 1908. Kieselhölzer der Steinkohlenformation und des Rotliegenden aus der bayerischen Rheinpfalz. Geognostische Jahreshefte 20: 1–16.Google Scholar
- Solomon, J.D. 1995. Guide to insect borers in North American broadleaf trees and shrubs. Agriculture handbook AH-706. Washington, D.C.: United States Department of Agriculture, Forest Service.Google Scholar
- Vité, J.P. 1952. Die holzzerstörenden Insekten Mitteleuropas, Textband. Göttingen: Musterschmidt.Google Scholar
- Weaver, L., S. McLoughlin, and A.N. Drinnan. 1997. Fossil woods from the Upper Permian Bainmedart Coal Measures, northern Prince Charles Mountains, East Antarctica. Journal of Australian Geology and Geophysics 16: 655–676.Google Scholar
- Witter, W., R. Witter, and C. Witter. 2011. Kieselhölzer aus dem Rotliegend von Crock in Südthüringen. Semana 26: 25–36.Google Scholar
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