Abstract
The occurrence of arthropods in amber exclusively from the Cretaceous and Cenozoic is widely regarded to be a result of the production and preservation of large amounts of tree resin beginning ca. 130 million years (Ma) ago. Abundant 230 million-year-old amber from the Late Triassic (Carnian) of northeastern Italy has previously yielded myriad microorganisms, but we report here that it also preserves arthropods some 100 Ma older than the earliest prior records in amber. The Triassic specimens are a nematoceran fly (Diptera) and two disparate species of mites, Triasacarus fedelei gen. et sp. nov., and Ampezzoa triassica gen. et sp. nov. These mites are the oldest definitive fossils of a group, the Eriophyoidea, which includes the gall mites and comprises at least 3,500 Recent species, 97% of which feed on angiosperms and represents one of the most specialized lineages of phytophagous arthropods. Antiquity of the gall mites in much their extant form was unexpected, particularly with the Triassic species already having many of their present-day features (such as only two pairs of legs); further, it establishes conifer feeding as an ancestral trait. Feeding by the fossil mites may have contributed to the formation of the amber droplets, but we find that the abundance of amber during the Carnian (ca. 230 Ma) is globally anomalous for the pre-Cretaceous and may, alternatively, be related to paleoclimate. Further recovery of arthropods in Carnian-aged amber is promising and will have profound implications for understanding the evolution of terrestrial members of the most diverse phylum of organisms.
Keywords: Acari, Cheirolepidiaceae, phytophagy, Carnian Pluvial Event
The oldest records of arthropods preserved in fossilized resin, or amber, until now have been from the Early Cretaceous of England, Japan, Lebanon, and Jordan (1–3), which coincides with the earliest appearances in the fossil record of large masses of resin ca. 130 million years (Ma) ago. This phenomenon is poorly understood, because resins have been produced since the Carboniferous (4) but usually in just trace quantities prior to the Cretaceous. Here we report the first arthropod inclusions in abundant Triassic amber, which extends the geological age of fossil arthropods in amber by approximately 100 million years. Two of the arthropods are members of the highly specialized mite lineage Eriophyoidea (5), which includes the gall mites and is thought to be ancient but lacks any other Mesozoic fossils.
The amber is from the middle part of the Heiligkreuz Formation, which is late Julian to early Tuvalian in age (Late Carnian: ca. 230 Ma), based on ammonites and palynology (6, 7). The outcrops occur near the village of Cortina in the Dolomite Alps of northeastern Italy (Fig. 1A). These appear to be the most abundant outcrops of Triassic amber in the world, with small droplets 2–6 mm (rarely to 30 mm) in diameter (Fig. 1F and Fig. S1) comprising 2–5% by volume of the paleosol in which they are buried. The amber was produced by trees in the extinct conifer family Cheirolepidiaceae (Fig. 1B) (6). That attribution is based both on chemistry of dispersed amber and on samples in situ within plant macrofossils, confirmed by abundant pollen and cuticles in the paleosols (Fig. 1 B–E). This amber has also yielded bacteria, algae, protists, and fungi (8).
Fig. 1.
Triassic (Carnian-aged) amber from the Heiligkreuz Formation of Cortina, northeastern Italy with associated plant and insect remains. (A) Location of amber outcrop (asterisk) in the Dolomite Mountains. (B) Cheirolepidiaceous shoots associated with amber. Museo delle Regole, Cortina d’Ampezzo, Italy, MRCA 7170. (C) Cuticle of the Cheirolepidaceae amber source. Department of Geology, Paleontology, and Geophysics, University of Padova, Italy, DGPGP ER-413c. (D) Cheirolepidiaceous foliage associated with in-situ amber. DGPGP ER-413d. (E) Resinous pocket in the foliage cuticle. DGPGP ER-365c. (F) Typical amber droplets. DGPGP ER-527. (G and H) Disarticulated nematoceran fly, showing details of antenna and apical tarsomere. Museum of Geology and Paleontology, University of Padova, Italy, MGP 31345. Scale bars: B, 2 cm; C–F, 1 mm; G and H, 200 μm.
Approximately 70,000 droplets (ca. 600–700 g) were screened for inclusions, from which three arthropods were discovered and prepared for microscopic study. One arthropod is a nematoceran fly (Diptera) (Fig. 1 G and H and Fig. S2) and the other two are highly divergent species of eriophyoid mites (Figs. 2 and 3). The midge specimen consists of portions of the head, antennae, thorax, and at least four legs. Most recent infraorders of Diptera (and some extinct ones) existed by the Late Triassic, even though Diptera only represented approximately 1% of all insect compressions during this time period (9). Many of the Triassic Diptera were quite small, which agrees with an estimated body length of the specimen reported herein, some 1.5–2 mm. The most intriguing feature of the midge is the pair of antennae with 10 compact, tapered segments (Fig. 1H), found sporadically in nematocerans and basal Brachycera. A detailed account of the specimen is given in SI Text.
Fig. 2.
Eriophyoid mite in the Italian Triassic amber: Triasacarus fedelei gen. et sp. nov., Holotype, MGP 31343. (A and C) Habitus in ventral view [reconstruction and photomicrograph, respectively; photo is a stacked image using differential interference contrast (DIC) illumination]. (B) Dorsal structures of anterior region, as viewed ventrally. (D) Gnathosoma, arrow pointing to infracapitular ledge [bright field (BF) illumination; f.p (focal plane) 2,347]. (E) Detail of F; arrows pointing to empodial featherclaws (BF, f.p. 2,324). (F) First and second leg pairs, with tip of proboscis in focus (arrow) and empodial featherclaw of first left leg indicated with arrow (BF, f.p. 2,324). (G) First and second leg pairs, with some solenidia denoted, tibial one by phi, tarsal ones by omega (DIC, f.p. 2,160). Scale bars: 10 μm.
Fig. 3.
Eriophyoid mite in the Italian Triassic amber: Ampezzoa triassica gen. et sp. nov., Holotype, MGP 31344. (A and B) Habitus, dorsal view. (A) Digitally stacked photomicrographic composite. (B) Rendering of complete specimen, as preserved. (C) Anterior portion of body, including gnathosoma. White arrows indicate infracapitular guides; black arrow points to second left leg (f.p. 2,904). (D) Portion of prodorsal and coxisternal region; arrows point to shadowy images of right legs I and II below prodorsal shield (f.p. 2,692). (E) Posterior apex of body; arrows point to caudal setae h2 (f.p. 2,932). All photos in DIC illumination. Scale bars: 10 μm.
The mite specimens are entire and preserved with microscopic fidelity (Figs. 2 and 3), such that they could be studied with compound microscopy up to x1,600 magnification. Although the two specimens are visible primarily on one surface, one mite is distinctively elongate and vermiform, with bizarre feeding structures, while the other is fusiform, more compact, with more integrated mouthparts. However, in general body form, with loss of the third and fourth pairs of legs, and presence of highly modified “featherclaws” on the remaining legs, there is no question as to their eriophyoid lineage placement (5).
Systematic Paleontology
Arachnida Cuvier, 1812; Acari Leach, 1817; Eriophyoidea Nalepa, 1898.
Triasacarus fedelei Lindquist and Grimaldi, gen. et sp. nov. (Fig. 2).
Etymology.
Generic from Triassic (geological period of origin) and acarus (Latin for mite); species name patronymic for Paolo Fedele (Cortina d’Ampezzo), discoverer of the Triassic amber deposit.
Holotype.
No. MPG 31343, Museum of Geology and Paleontology, University of Padova.
Locality and horizon.
Heiligkreuz Formation, Late Carnian.
Diagnosis.
Body length 210 μm, body shape vermiform; gnathosomatic infracapitulum framed by palpcoxal bases, from which other palpal segments extend freely, on either side of a long proboscis, flanked dorsally by pair of acuminate, possibly cheliceral structures; prodorsal shield with frontal lobe and one pair of setae inserted anterolaterally and one pair inserted posteriorly; opisthosoma with ca. 55–60 fine annuli circumscribing body, not broadened into tergites dorsally; each with single transverse row of minute spicules; opisthosoma with prominent pair of subcaudal setae f and with ventrolateral setae d, e, and caudal setae h1 and h2 seemingly evident; legs I and II with long empodial featherclaws, main shafts divided; legs I and II with a prominent seta on each of femur, genu, tibia (two setae), and a short seta on tarsus (not verifiable on leg I); leg II with a probable solenidion on each of tibia and tarsus (not verifiable on leg I); legs III–IV absent. Detailed description provided in SI Text.
Ampezzoa triassica Lindquist and Grimaldi, gen. et sp. nov. (Fig. 3).
Etymology.
Generic from Valle d’Ampezzo in northeastern Italy, source of Triassic amber outcrops; species name for period of geological origin.
Holotype.
No. MPG 31344, Museum of Geology and Paleontology, University of Padova.
Locality and horizon.
Heiligkreuz Formation, Late Carnian.
Diagnosis.
Body length 124 μm; body shape fusiform, dorsoventrally flattened, gnathosomatic infracapitulum framed by adherent inner margins of palpal segments, between which a gutter bears a set of indistinguishable structures (some cheliceral); prodorsal shield with an unpaired anteromedian seta, one pair of setae inserted midlaterally, and one pair inserted on pair of closely set dorsal tubercles posteriorly. Opisthosoma with ventral annuli broadened into ca. 18 tergites, 1–15 bear pair of digitiform, apparently wax-secreting lateral lobes; with prominent pair of caudal setae h2 and with ventrolateral setae d, e, f, and accessory caudal setae h1 seemingly evident. Leg I with long, slender tarsus, its empodial featherclaw with main shaft possibly divided; with 5 discernible setae, one each seems to occur on femur, genu, tibia, tarsus, and a second one on tarsus; tarsal solenidion with enlarged tip, tibial solenidion indiscernible. Leg pair II present but structure not discernible; legs III–IV absent. Detailed description provided in SI Text.
Discussion
Both rounded, vermiform, and flattened, fusiform gall mites occur throughout disparate genera of the three extant families of Eriophyoidea. Vermiform mites generally live in sequestered spaces (sheaths, galls, buds) that protect them from desiccation, while a fusiform body correlates with a vagrant lifestyle on exposed surfaces of plants. Ampezzoa displays faint, parallel striations that extend over the dorsum of the body and do not appear to be cuticular (Fig. 3 A and B). We interpret these striations as waxy filaments, secretion of which occurs sporadically in vagrant Eriophyoidea (5). In fact, the modern New Zealand species Cymeda zealandica Manson & Gerson, which feeds on tree ferns, also has lateral fringes of wax and a body shape very similar to this Triassic species. Just as in other terrestrial arthropods, secretions of flocculent wax are believed to be an adaptation of external plant feeders against desiccation, rain, predation, and parasitism.
The fossils reported here extend the geological record of the eriophyoid lineage by approximately 185 Ma. They cannot be assigned to any of the three extant families, partly due to inadequate classification in this superfamily, as well as to some unusual attributes of the fossils. The very divergent body structure of the fossils indicates they are distantly related, which is further supported by Triasacarus lacking integrated feeding appendages. This, and the presence of a tibial solenidion on leg II in Triasacarus (Fig. 2 A and G), are plesiomorphically unique in the lineage Eriophyoidea. It is very possible that this taxon is a stem group eriophyoid, indicating that significant divergence occurred in Eriophyoidea prior to the Late Triassic.
The Eriophyoidea is the most highly specialized lineage of phytophagous mites, indeed of any arthropods except certain insects such as scales (Hemiptera: Coccoidea). Most eriophyoid species are extremely host specific, typically confined to a species or genus of host plants (5). Despite the common name of gall mites, only about one-third of the species actually induce formation of galls or other abnormal plant growths. The remaining species are leaf vagrants or they live sequestered within sheaths, buds, and flowers. Of the ca. 3,500 described species of extant world eriophyoids, 97% use angiosperms as hosts (5); the other 3% feed on conifers and ferns, with even two mite species feeding on Ephedra and Equisetum, respectively. Fern feeding is considered to be secondary (5), because all are disparate species in 11 genera of the more derived family Eriophyidae.
Feeding on conifers is typically interpreted as an ancient association in Eriophyoidea (5), because half of the extant species in the putatively primitive family Phytoptidae subsist on conifers. Of the conifer hosts, more than 90% are Pinaceae and Cupressaceae. Only one eriophyoid, Pentasetacus araucariae Schliesske, is presently known to feed on the relict conifer family Araucariaceae, and that mite is morphologically quite primitive (10, 11). Monocotyledonous plants have also been considered as a group of hosts upon which eriophyoid mites arose, because several putatively early derivative genera of Phytoptidae are restricted to palmaceous or graminaceous hosts (5).
The Triassic fossils clearly reveal that eriophyoids preceded angiosperms by at least 100 million years and fed on conifers. There is evidence that the tiny amber droplets from the Heiligkreuz Formation were formed on the leaf surfaces of the source cheirolepidiaceous tree (7) (Fig. 1 D and E), so it is likely that the fossilized mites were either sheath dwellers or surface vagrants feeding on the foliage. Mites like Triasacarus may have produced galls, as some of the morphologically most primitive forms of extant vermiform mites induce galls on twig and bark surfaces of their conifer hosts (10, 12). Also, some conifer-feeding eriophyoids today cause leaf/needle yellowing, browning, necrosis, dehiscence, and even russetting and deformation, so it is possible that the fossil mites induced formation of the Triassic amber droplets, although we are unaware of any eriophyoids today inducing resin production.
The discovery of eriophyoid mites in Triassic amber substantiates the lineage’s antiquity, in contrast to some previous notions about this being a more recently derived group linked with tetranychoid (spider mites and relatives) or other raphignathine superfamilies (5). The fossils further demonstrate eriophyoids as ancient because they had already achieved their specialized body plan by the Triassic, especially the loss of the third and fourth pairs of legs. The current notion is thus exceedingly unlikely of finding a transitional extant form (that retains at least the third pair of legs) on some unsampled primitive conifer such as one of the Araucariaceae (13). Whether this obligate plant-feeding lineage of mites preceded the origin of the conifers in the Late Carboniferous, ca. 300 Ma, becomes a new speculation, specifically if Paleozoic progymnosperms or early seed ferns were ancestral host plants.
The Triassic eriophyoid mites provide additional evidence for the antiquity of acariform mites (subclass Acari, superorder Acariformes), which have a fossil record beginning in the Early Devonian (14, 15), although records of Carboniferous, Triassic, and Jurassic mites are scarce. Mites in Cretaceous and Cenozoic amber are very diverse (3, 5, 16), albeit poorly studied, and virtually all of them belong to modern families. The Triassic amber gall mites confirm the hypothesized antiquity of Trombidiform mites (a lineage within Acariformes that includes the Eriophyoidea), which were estimated to have diverged in the Devonian based on molecular evidence (17). The only other definitive fossil Eriophyoidea is a specimen preserved as cuticle in clay from the Middle Eocene of South Australia (18). A few galls on fossil leaves from the Cenozoic have been attributed to eriophyoid mites (19, 20) and galls on gnetopsid and peltasperm plants from the Late Triassic have been attributed to “foliar gall mites” (21), although these records lack definitive evidence of mites themselves.
Interestingly, virtually all amber recovered from the Triassic occurs within the narrow 10-million-year interval of the Carnian, 230 Ma (Fig. S3). Widespread amber occurrence during this time period may be a result of the Carnian Pluvial Event (7, 22), a global episode of atmospheric perturbation linked to massive volcanism associated with the Wrangellian Large Igneous Province (23) as well as profound changes in a monsoonal climate (7, 24). The Cheirolepidiaceae plant remains in the amber-bearing paleosol, primarily cuticles with possible affinities to the genera Brachypyllum and Pagiophyllum (25), exhibit the typical xerophytic features of this family (6, 7); however, the dominance of hygrophytic forms in the palynological morphospecies found generally in the Carnian suggests climate changes. The decrease of xerophytic taxa and the increase of hygrophytic associations attributable to ferns, clubmosses, horsetails, and the Cycadeoidales indicate multiple humid climate pulses within the Carnian Pluvial Event (7). Paleosol analyses confirmed that this climatic event can be considered as a supraregional climate shift with increased rainfall during the late Early Carnian, followed by a decrease in the Late Carnian (22). Such a climate is probably ideal for the secretion of large amounts of resins (6, 7, 26) as well as for the formation of fluvial sediments that optimally preserve amber. Perhaps a similar climatic change is responsible for the enigmatic abundance of amber beginning in the Early Cretaceous, although other hypotheses include the advent of certain conifers, along with groups of wood-infesting beetles and fungi (27).
The Triassic is a transformative period in the evolutionary history of terrestrial arthropods, because taxa from this period are much more modern in their relationships than are taxa from the Permian (1). Indeed, the earliest representatives of the insect orders Diptera, Hymenoptera, Thysanoptera (thrips), and Trichoptera (caddisflies) are Triassic, which is also when diverse crown-group beetles (Coleoptera) appear. Presumably, the end-Permian extinctions had a significant effect on insects (1). The discovery of other significant terrestrial arthropods in the Triassic Italian amber is very promising. Although size of inclusions within amber droplets is limited to 1–3 mm, diverse arthropods occur in this body size. In particular, Sternorrhyncha (a group that includes modern whiteflies, aphids, and scale insects), Psocodea (bark lice), and Thysanoptera (thrips) are typically small insects living on plant surfaces, for which stem-group Triassic species occur as compressions (1). Given the microscopic fidelity of preservation within amber, any specimens of these insect groups in Dolomite amber would greatly illuminate their early evolution.
Materials and Methods
Collection and Screening.
Amber-bearing paleosol was field collected and elutriated in water; amber droplets were separated from plant remains and placed in water on glass microscope slides with moulds (Menzel Inc.), covered by a glass coverslip and screened for inclusions under a Carl Zeiss AxioScope A1 compound microscope.
Preparation.
Three small amber droplets, approximately 3 mm in diameter and 2–3 mm in length, each containing an arthropod, were individually embedded in a high-grade epoxy resin (Buehler Epoxicure), in a procedure modified from the protocols described in ref. 28. Samples were trimmed and polished on opposite sides using a series of emery papers with decreasing grit sizes (P1200, P1500, P2500: Buehler) on a Buehler Ecomet-3 variable speed flat lapidary wheel, with a fine stream of water. The amber surface was gradually removed from opposite sides of each amber droplet, such that flattened surfaces were parallel to the broadest surfaces of each arthropod inclusion; each flattened surface was brought to about 100 μm of the inclusion to optimize microscopic examination.
Photomicrography.
Prepared specimens were applied to a glass microscope slide with a drop of water, with another drop applied to the upper surface of the amber, covered with a 0.06–0.08 mm thickness glass coverslip (Menzel Inc.). This reduces light scattering from fine surface scratches and improves optical resolution (contact of the amber with oil or organic liquid should be avoided because it may be deleterious to the amber). Optical immersion oil was allowed to contact only the glass coverslip, not the amber surface. Specimens were photographed with a Carl Zeiss AxioScope A1 compound microscope, using 640 to 1,600x (oil immersion) magnification and either bright field (BF) or differential interference contrast (DIC) illumination. A series of over 3,000 individual photomicrographs were taken of the three specimens at various magnifications and in successive focal planes using a Canon 450 D digital camera; images were then digitally compiled using Helicon Focus 5.0 software. Finest structures, such as fine setae, were best resolved using individual slices/photos, so for the descriptions of the eriophyoid mites (e.g., Figs. 2 and 3) individual focal planes (“f.p.”) are referenced when discussing certain structures. The complete set of digital image files is available to qualified researchers upon request to the corresponding author. Illustrations were made by first tracing high-resolution printouts of images compiled from the stacked images, then filling in details using the photos from individual focal planes taken at 1,600x magnification (which had the greatest resolution), as well as with direct observation of the specimens under 1,000x magnification using a Nikon Eclipse E600 compound microscope. Morphological terminology follows that of Lindquist (5) for the Eriophyoidea, and (29) for the midge.
Supplementary Material
ACKNOWLEDGMENTS.
We thank A. Busch (Göttingen), S. Castelli (Padova), O. Coppellotti (Padova), P. Fedele (Cortina d’Ampezzo), P. Gianolla (Ferrara), S. Perkins (New York), V. Perrichot (Rennes), E.-M. Sadowski (Göttingen), W. Schönborn (Jena), and S. Thurston (New York) for their assistance with this work. This is publication number 86 from the Courant Research Centre Geobiology, funded by the German Initiative of Excellence.
Footnotes
The authors declare no conflict of interest.
*This Direct Submission article had a prearranged editor.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1208464109/-/DCSupplemental.
References
- 1.Grimaldi DA, Engel MS. Evolution of the Insects. Cambridge, UK: Cambridge Univ Press; 2005. p. 755. [Google Scholar]
- 2.Martínez-Delclòs X, Briggs DEG, Peñalver E. Taphonomy of insects in carbonates and amber. Palaeogeogr Palaeoclimatol Palaeoecol. 2004;203:19–64. [Google Scholar]
- 3.Penney D, editor. Biodiversity of Fossils in Amber. Manchester, UK: Siri Scientific Press; 2010. p. 304. [Google Scholar]
- 4.Bray PS, Anderson KB. Identification of Carboniferous (320 million years old) class Ic amber. Science. 2009;326:132–134. doi: 10.1126/science.1177539. [DOI] [PubMed] [Google Scholar]
- 5.Lindquist EE, Sabelis MW, Bruin J, editors. Eriophyoid Mites: Their Biology, Natural Enemies, and Control. Amsterdam: Elsevier; 1996. p. 790. [Google Scholar]
- 6.Roghi G, Ragazzi E, Gianolla P. Triassic amber of the Southern Alps (Italy) Palaios. 2006;21:143–154. [Google Scholar]
- 7.Roghi G, et al. Palynological correlation of Carnian humid sub-events throughout western Tethys. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;290:89–106. [Google Scholar]
- 8.Schmidt AR, Ragazzi E, Coppellotti O, Roghi G. A microworld in Triassic amber. Nature. 2006;444:835. doi: 10.1038/444835a. [DOI] [PubMed] [Google Scholar]
- 9.Blagoderov V, Grimaldi D, Fraser NC. How time flies for flies: Diverse Diptera from the Triassic of Virginia and early radiation of the order. Am Mus Novit. 2007;3572:1–39. [Google Scholar]
- 10.Schliesseke J. Distribution and ecology of a new ancestral species of gall mites (Acari: Eriophyoidea) Entomol Mitt Zool Mus Hamburg. 1985;8:97–106. , German. [Google Scholar]
- 11.Shevchenko VG, Bagnyuk IG, Sukhareva SI. A new family of four-legged mites, Pentasetacidae (Acariformes, Tetratpodili) Zool Zh. 1991;70:47–53. , Russian. [Google Scholar]
- 12.Shevchenko VG, Bagnyuk IG, Rinne V. Trisetacus pini (Nalepa, 1889) in some Baltic countries and in Russia (taxonomy, morphology, biology, distribution) Acarina. 1993;1:51–71. [Google Scholar]
- 13.Lindquist EE. In: Acarology: Proceedings of the 10th International Congress 1998, Canberra, Australia. Halliday RB, et al., editors. Melbourne: CSIRO Publishing; 2001. pp. 17–34. [Google Scholar]
- 14.Labandeira CC, Phillips TL, Norton RA. Oribatid mites and the decomposition of plant tissues in Paleozoic coal-swamp forests. Palaios. 1997;12:319–353. [Google Scholar]
- 15.Subías LS, Arillo A. Oribatid mite fossils from the Upper Devonian of South Mountain, New York and the Lower Carboniferous of County Antrim, Northern Ireland (Acariformes, Oribatida) Est Mus Cien Nat de Alava. 2002;17:93–106. [Google Scholar]
- 16.Dunlop JA, Penney D, Jekel D. In: A summary list of fossil spiders and their relatives. Platnick NI, editor. New York: American Museum of Natural History; 2012. pp. 1–261. available at http://research.amnh.org/entomology/spiders/catalog/index.html. [Google Scholar]
- 17.Dabert M, et al. Molecular phylogeny of acariform mites (Acari, Arachnida): Strong conflict between phylogenetic signal and long-branch attraction artifacts. Mol Phyl Evol. 2010;56:222–241. doi: 10.1016/j.ympev.2009.12.020. [DOI] [PubMed] [Google Scholar]
- 18.Southcott RV, Lange RT. Acarine and other microfossils from the Maslin Eocene, South Australia. Rec S Aust Mus. 1971;16:1–21. [Google Scholar]
- 19.Heyden C. Arthropods from the brown coal of the Lower Rhine, Wetterau and Rhön areas. Palaeontographica. 1862;10:62–82. , German. [Google Scholar]
- 20.Scott AC, Stephenson J, Collinson ME. In: Plant Galls. Williams MAJ, editor. Oxford: Clarendon Press; 1994. pp. 447–470. [Google Scholar]
- 21.Labandeira CC. Silurian to Triassic plant and hexapod clades and their associations: New data, a review, and interpretations. Arthr Syst Phyl. 2006;64:53–94. [Google Scholar]
- 22.Breda A, et al. The Carnian Pluvial Event in the Tofane area (Cortina d‘Ampezzo, Dolomites, Italy) Geo Alp. 2009;6:80–115. [Google Scholar]
- 23.Dal Corso J, et al. Discovery of a major negative δ13C spike in the Carnian (Late Triassic) linked to the eruption of Wrangellia flood basalts. Geology. 2012;40:79–82. [Google Scholar]
- 24.Preto N, Kustatscher E, Wignall PB. Triassic climates—State of the art and perspectives. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;290:1–10. [Google Scholar]
- 25.Roghi G, Kustatscher E, Van Konijnenburg-Van Cittert JHA. Late Triassic Plants from the Julian Alps (Italy) Boll Soc Paleontol It. 2006;45:133–140. [Google Scholar]
- 26.Langenheim J. Plant Resins: Chemistry, Evolution, Ecology, and Ethnobotany. Portland, OR: Timber Press; 2003. [Google Scholar]
- 27.McKellar RC, et al. Insect outbreaks produce distinctive carbon isotope signatures in defensive resins and fossiliferous ambers. Proc R Soc Biol Sci Ser B . 2011;278:3219–3224. doi: 10.1098/rspb.2011.0276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Nascimbene P, Silverstein H. In: Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey, Grimaldi D, editor. Leiden, The Netherlands: Backhuys Publishers; 2000. pp. 93–102. [Google Scholar]
- 29.McAlpine JF. In: Manual of Nearctic Diptera. McAlpine JF, et al., editors. Vol. 1. Ottawa: Agriculture Canada; 1981. pp. 9–64. [Google Scholar]
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