Current Biology 24, 1606–1610, July 21, 2014 ª2014 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2014.05.048 Report A Diverse Paleobiota in Early Eocene Fushun Amber from China

Bo Wang,1,2,* Jes Rust,2 Michael S. Engel,3 Jacek Szwedo,4 regarded as an important source of medicine and organic Suryendu Dutta,5 Andre´ Nel,6 Yong Fan,7 Fanwei Meng,1 gemstones. The inclusions, however, were not the subject of Gongle Shi,1 Edmund A. Jarzembowski,1,8 a comprehensive investigation, and its paleobiota and scienti- Torsten Wappler,2 Frauke Stebner,2 Yan Fang,1 Limi Mao,1 fic significance were inevitably overlooked in almost all main- Daran Zheng,1 and Haichun Zhang1,* stream paleontological literature [1, 5]. Fushun amber contains 1State Key Laboratory of Palaeobiology and Stratigraphy, the only Paleogene Asian (Laurasia-originated) arthropod Nanjing Institute of Geology and Palaeontology, Chinese biota that has sufficiently numerous and diverse fossils to Academy of Sciences, Nanjing 210008, China permit detailed investigation. It not only fills a crucial biogeo- 2Steinmann Institute, University of Bonn, 53115 Bonn, graphic gap in Eurasia but also spans the Early Eocene Cli- Germany matic Optimum (EECO), which is considered an important 3Division of Entomology, Natural History Museum, and analog for inferring future effects of warming trends on biotic Department of Ecology and Evolutionary Biology, University of interactions [12–14], making it a vital source of information Kansas, Lawrence, KS 66045, USA for biotic change during the Paleogene. 4Department of Zoology and Parasitology, University of Gdansk, 59 Wita Stwosza Street, 80-308 Gdansk, Poland Geological Context 5Department of Earth Sciences, Indian Institute of Technology The mining district in the Fushun basin is located to the south Bombay, Powai, Mumbai 400076, India of Fushun City, Liaoning Province, China (Figure 1). The sedi- 6CNRS UMR 7205, CP 50, Entomologie, Muse´ um National mentary fill in this basin contains the Paleocene Laohutai d’Histoire Naturelle, 75005 Paris, France and Lizigou Formations and the Eocene Guchengzi, Jijuntun, 7Fushun Amber Institute, Fushun 113005, China Xilutian, and Gengjiajie Formations (Figure 1). The Eocene Gu- 8Department of Earth Sciences, Natural History Museum, chengzi Formation includes thick coal beds intercalated with London SW7 5BD, UK carbonaceous shale. Fushun amber comes from the middle and upper coal beds of the Guchengzi Formation in the West Opencast Coalmine, which is the largest opencast coalmine Summary in Asia (Figure S1 available online). After more than 110 years of mining, the opencast mine is closing at Fushun, ending Paleogene arthropod biotas have proved important for the supply of amber. We now have a final opportunity to study tracing the faunal turnover and intercontinental faunal inter- this fossil resin and its inclusions before local knowledge fades change driven by climatic warming and geodynamic events and collections are dispersed. [1–5]. Despite the large number of Paleogene fossil arthro- The amber-bearing strata have been assigned an early-mid- pods in Europe and North America [5–8], little is known about dle Ypresian age (50–53 mega-annum [Ma]), constrained by the the typical Asian (Laurasia-originated) arthropod biota. Here, paleofloras [16, 17], paleomagnetic considerations [16], and we report a unique amber biota (50–53 million years ago) from isotopic dating (Supplemental Results and Discussion)[16]. the Lower Eocene of Fushun in northeastern China, which Paleobotanical and geochemical data suggest that the Early fills a large biogeographic gap in Eurasia. Fushun amber Eocene paleoclimate in Fushun was moist subtropical [17, 18]. is derived from cupressaceous trees, as determined by gas chromatography-mass spectrometry, infrared spectroscopy, Amber Characteristics and paleobotanical observations. Twenty-two orders and Fushun amber is frequently translucent and reddish or more than 80 families of arthropods have been reported so yellowish in color (Figure S2). The amber pieces are usually far, making it among the most diverse amber biotas. Our re- small and seldom longer than 10 cm. The amber-bearing sults reveal that an apparent radiation of ecological keystone coal deposits were affected by a massive intrusion of basic insects, including eusocial, phytophagous, and parasitoid magmas in the Oligocene; therefore, the amber was heated dur- lineages, occurred at least during the Early Eocene Climatic ing diagenesis. The Fourier transform infrared (FTIR) spectrum Optimum. Some insect taxa have close phylogenetic affin- of Fushun amber shows characteristics of cupressaceous- ities to those from coeval European ambers, showing a biotic araucarian resins [19]. For example, the amplitude of the ab- interchange between the eastern and western margins of the sorption peak at 1,385 cm21 is lower than the adjacent peak Eurasian landmass during the Early Paleogene. at 1,460 cm21, and the absorption peak at 791 cm21 is present [19, 20](Figure S3). The total extracts of Fushun amber were Results and Discussion analyzed by gas chromatography-mass spectrometry (GC- MS) (Figure 2). The presence of abietane-type diterpenoids of Amber-bearing deposits are among the most important Kon- Fushun amber extracts is diagnostic of a coniferous source servat-Lagersta¨ tten, providing unique windows into past eco- [21–23], and the absence of plant triterpenoids clearly excludes systems [9–11]. Here, we report on a unique amber biota from an angiosperm origin. The phenolic diterpenoids, such as ferru- the Lower Eocene of Fushun in northeastern China. Fushun ginol and 12-hydroxysimonellite, are of significant chemotaxo- amber has been known for over a century and was traditionally nomic value because these biomarkers are detected in the extant coniferous families Cupressaceae and Podocarpaceae [21, 24]. The absence of tetracyclic diterpenoids (i.e., kaurane *Correspondence: [email protected] (B.W.), [email protected] and phyllocladene) suggests a minimal contribution from Podo- (H.Z.) carpaceae [22, 25]. Dehydroabietane, a natural product of many Fushun Amber Biota 1607

Figure 1. The Paleogeographic Setting of Northeastern China during the Eocene and the Stratigraphic Sequence of the West Opencast Coalmine Paleogeographic setting of northeastern China during the Eocene (left); stratigraphic sequence of the West Opencast Coalmine (right). Yellow areas denote former mountain ranges; green areas denote coal-bearing basins; blue areas denote sea (paleotopographic information from Wang [15]). Red pentagon indicates fossil layers yielding macrofossils; red stars represent amber layers. PETM, Paleocene-Eocene Thermal Maximum (approximately 55 Ma); EECO, Early Eocene Climatic Optimum (51–53 Ma).

(16%), and Hemiptera (11%) (Fig- ure 3). Diptera are mainly composed of nonbiting midges (mainly Chironomi- dae: Orthocladiinae) and dark-winged fungus gnats (Sciaridae). Hymenoptera are largely represented by ants and various parasitoid wasps. Hemiptera are mainly composed of aphids (mainly Drepanosiphidae, Phloeomyzidae, and Eriosomatidae). Interestingly, beetles, which dominate in numbers of species today, comprise only 2% of all insect inclusions.

Paleoecology and Biogeography Some insects in Fushun amber are related to those from extant subtropical Pinaceae and Cupressaceae resins [24], is the most dominant or tropical Asian ecosystems. For example, the aphid genus compound in the extracts of Fushun amber. However, the Yueaphis is related to Recent Southeast Asian genera (e.g., phenolic abietanes of Fushun amber are not detected in the Astegopterys, Ceratovacuna, and Neothoracaphis)[27]. In- resins of Pinaceae [21, 25]. Consequently, chemical analysis sects with aquatic or semiaquatic larval stages (i.e., nonbiting shows that dominance of dehydroabietane and subordinate midges, mayflies, and moth flies; Figures 3C and S4B) and phenolic diterpenoids (such as ferruginol and 12-hydroxy- aquatic microorganisms (i.e., testate amoebae) are common, simonellite) points to amber derivation from cupressaceous consistent with a humid environment in the Eocene Fushun coniferous trees. This is consistent with FTIR spectroscopy. forest [28]. Thus, the insect inclusions confirm a moist and Cupressaceae (especially Metasequoia) are not only the most warm Early Eocene climate in the Fushun area. common plant inclusions in Fushun amber (Figure 3A) but Ants (Formicidae) are the most diverse eusocial insects also very frequent as compressions in the amber-bearing and in Fushun amber (Figure 3E). Our preliminary investigation succeeding layers, supporting the chemical interpretation. reveals at least four subfamilies, which is consistent with a subtropical climate: Myrmecinae, Ponerinae, Formicinae, Paleobiota and Dolichoderinae. The increased percentage of ants in Fushun amber contains a diverse fossil arthropod fauna Fushun amber (5% of all insects) over Oise amber (<2.5%), and abundant botanical and other inclusions, such as fungi on par with Baltic amber (5%), is in accordance with the and even mammalian hairs. In addition, some microinclusions, general pattern of ant abundance increasing during the such as palynomorphs and testate amoebae, are frequently Paleogene, particularly during the EECO [29]. Fushun amber found (as in Figure S4H) [26]. Arthropod inclusions cover an contains many aphids, one small piece preserving 43 wingless impressive array, including 22 orders and more than 80 fam- female individuals (Figure 3B), which is similar to living popu- ilies. They currently comprise the Diplopoda, the arachnid lations. Extant aphid families had already appeared during orders Acariformes, Parasitiformes, Araneae, Opiliones, and the Cretaceous but were rare, whereas most Mesozoic aphids Pseudoscorpiones, and at least 70 families of Insecta in 16 or- belong to extinct families [30]. In contrast, almost all of the ders (Figure S4; Table S2; Supplemental Results and Discus- Fushun aphids belong to extant families (i.e., Drepanosiphi- sion). As in other amber deposits, large arthropods are very dae, Phloeomyzidae, and Eriosomatidae), showing remark- rare in Fushun amber, and more than 99% of the inclusions able resemblance to the Recent fauna and suggesting that are less than 1 cm in length. Spiders and mites are frequent in the radiation of modern aphid clades occurred during the Fushun amber. Most spiders are strongly deformed and appear EECO or just prior to it. to be juveniles or females (Figure S4C). The insect fauna is Although parasitoid insects are already known from Creta- dominated by Diptera (70% of all 2,780 insects), Hymenoptera ceous amber deposits [6], their high diversity in Fushun amber Current Biology Vol 24 No 14 1608

differences probably resulted in the observed difference between the Fushun and Cambay ambers. In the Cretaceous and Early Paleogene, the Eurasian land- mass was divided by the epicontinental Turgai Sea (Figure 4), which represented an important dispersal barrier for the terrestrial and limnic faunas [2]. Although it has been sug- gested that Early Palaeogene Eurasian dispersal had indeed taken place [13, 36], little fossil evidence supporting this assumption has been reported. Almost all Eurasian biotic interchange was thought to have occured after the closing of the Turgai Sea (approximately 30 Ma) [14, 37]. Surprisingly, some taxa in Fushun amber have phylogenetic affinities with organisms from coeval European ambers. One example is the scuttle fly (Phoridae) genus Eosciadocera, which only oc- curs in Fushun and Baltic ambers [38]. Another phorid genus, Rhoptrocera, is closely related to Pararhoptrocera from the Paleocene or Early Eocene amber of the Czech Republic [39]. A new species of Psyllipsocus (a representative of the Figure 2. Ion Chromatograms of Fushun Amber rare psocodean family Psyllipsocidae) in Fushun amber is (A) Total ion chromatograms of the total extracts. Black circles indicate long chain alkanes. very similar to Psyllipsocus eocenicus in Oise amber (Fig- (B) Selected ion chromatograms (mass/charge ratio [m/z] 268 + 286) dis- ure S4I) [40]. Another interesting example is a minute false playing the presence of ferruginol and 12-hydroxysimonellite. fairy wasp (Mymarommatidae) belonging to Palaeomymar, The major compounds are diterpenoids with minor sesquiterpenoids. previously known only from Baltic amber (Figure 3F) [41]. The major diterpenoids include abietane, 19-norabieta-8,11,13-triene, de- This evidence implies a biotic link between Fushun and coeval hydroabietane, simonellite, abieta-8,11,13 triene, abieta-8,11,13 trien-7- European ambers, either representing lineages that were more one, ferruginol, and 12-hydroxysimonellite (Table S1). Bicyclic compounds such as octahydro-tetramethyl naphthalene and their isomers are detected ancient and widespread before the opening of the Turgai Sea in subordinate amounts. Major sesquiterpenoids are ionene and methyl (approximately 180 Ma [2]) or that were, more likely, some ionene. form of biotic exchange by oceanic dispersal [42] or through temporary land bridges [13]. In addition, there are many taxa in Baltic amber that have living relatives in Southeast Asia, is a remarkable discovery, which for the Cenozoic is compara- suggesting that insect taxa probably had much wider distri- ble with Baltic amber. A male twisted-winged parasite (Strep- butions in the Paleogene [43]. Therefore, biotic interchange siptera) has been recovered (Figure 3G). Strepsiptera are an during the Paleogene seems likely between the eastern and enigmatic order of minute entomophagous parasitoids whose western margins of the Eurasian landmass. phylogenetic affinities remain unclear, although they are prob- Our study provides the first detailed, comprehensive inves- ably related to beetles [31]. They are exceedingly rare in the tigation for the Fushun amber. So far, we have found abundant fossil record, with Cenozoic fossils only in Eocene Baltic arthropod inclusions belonging to more than 80 families, amber, Messel oil shale from Germany, and Miocene amber making it among the most diverse amber biotas. In spite of from the Dominican Republic [32]. Fushun amber also pre- the cessation of mining operations, the already-gathered serves diverse parasitoid wasps, including Ichneumonidae, material is being studied and holds the potential for a deeper Braconidae, and Mymarommatidae (Figures 3F and S4F). understanding of Paleogene biogeography and environmental Some of these minute insects, rarely found as compression change. fossils, should help to resolve the phylogeny and timescale of wasp evolution and parasitoid behavior. Another interesting Experimental Procedures discovery is a pair of mating nonbiting midges (Chironomidae) surrounded by several unpaired individuals (Figure 3C), indic- Microscopy and FTIR Spectroscopy ative of a mating swarm, which is also known from Baltic Fresh amber is coated in thick coal dust, so pieces were ground and pol- ished manually with a series of wet silicon carbide abrasive papers to re- amber [6]. Other significant insects include mayflies (Ephemer- move the opaque surface and to minimize light scattering during further optera: Philolimniidae), barklice (Psocodea: Psyllipsocidae, investigation. The pieces with inclusions were cut into smaller samples Mesopsocidae), and thrips (Thysanoptera: Phlaeothripidae), and trimmed using a shaving blade and then polished using diatomite pow- revealing that these lineages radiated at least during the der. The specimens were examined under a Nikon SMZ1000 stereomicro- EECO (Figures 3D and 3H). scope and a Zeiss Discovery V20 microscope. Photographs were taken During the Paleogene period, insect biotas, preserved as with a Nikon DXM1200 digital camera that was connected to the Nikon ste- reomicroscope and the Zeiss Discovery V20 system mentioned above. FTIR amber inclusions or compressions, were widespread in North spectroscopy was conducted with a Thermo Scientific Nicolet iS10 spec- America and Europe [5–8, 33](Figure 4). At least 14 Paleogene trometer. All amber inclusions are deposited in the Nanjing Institute of amber biotas have been found around the world, but most Geology and Palaeontology (NIGP), Chinese Academy of Sciences (CAS). of them remain poorly investigated (e.g., Sakhalin amber [5], Arkansas amber [7], and British Columbia amber [8]; Supple- Chemical Analysis mental Results and Discussion). There are no shared or similar Handpicked amber samples were solvent extracted with a dichloromethane species so far between Fushun and contemporaneous Cam- and methanol (ratio 9:1) mixture. The amber pieces were kept inside the bay amber, which is associated with a tropical dipterocarpa- solvent mixture for 24 hr and then extracted ultrasonically for 1 hr. The total extracts were analyzed by GC-MS with an Agilent 7890A chromatograph ceous rainforest [1]. The initial India-Asia collision is estimated interfaced with an Agilent 5975C MSD at the Indian Institute of Technology at approximately 50 Ma [35], but the biotic interchange prob- Bombay. The gas chromatograph (GC) was fitted with an HP-5MS fused ably began earlier [1]. Therefore, the climatic and vegetational silica capillary column (30 m 3 0.25 mm internal diameter, 0.25 mm film Fushun Amber Biota 1609

Figure 3. Representative Plants and Arthropods in Fushun Amber (A) Metasequoia leaf, NIGP156966. (B) Aphid swarm, NIGP156967. (C) Nonbiting midges (Diptera: Chironomidae), NIGP156968. A pair of mating midges facing in opposite directions, with the same body orien- tation (ventral surfaces facing in the same direc- tion), is shown. (D) Thrips (Thysanoptera: Phlaeothripidae), NIGP156969. (E) Ant (Hymenoptera: Formicidae), NIGP156970. (F) False fairy wasp (Hymenoptera: Mymaromma- tidae), NIGP156971. (G) Twisted-winged parasite (Strepsiptera), NIGP156972. (H) Barklouse (Psocodea: Mesopsocidae), NIGP156973. Scale bars of (A)–(C) and (H) represent 2 mm. Scale bars of (D)–(G) represent 0.5 mm.

thickness). Helium was used as the carrier gas at a flow rate of 1 ml/min. The Supplemental Information GC oven temperature was held at an initial 40C for 5 min and then ramped to 310Cat4C/min, which was held for a final 5.5 min. Full scan (mass/ Supplemental Information includes Supplemental Results and Discussion, charge ratio [m/z] 40 2 600) 70 eV mass spectra were acquired with a source four figures, and two tables and can be found with this article online at temperature of 300C. http://dx.doi.org/10.1016/j.cub.2014.05.048.

Figure 4. Paleogeographic Locations of Major Paleogene Insect Faunas A, Early Eocene Fushun amber in China (50–53 Ma); B, Early Eocene Cambay amber in India (50–52 Ma); C, Eocene Rovno amber in Ukraine (33–40 Ma); D, Eocene Baltic amber (including Bit- terfeld amber; 33–40 Ma); E, Early Eocene Oise amber in France (53 Ma); F, Early Eocene British Columbia amber in Canada (50–55 Ma); G, Early Eocene Arkansas amber in USA (50 Ma); H, Middle Eocene Eckfeld/Messel shale in Germany (44–48 Ma); I, Early Eocene Fur Formation in Denmark (54–56 Ma); J, Late Eocene Bembridge Marls of the Isle of Wight, UK (36 Ma); K, Early Eocene Oka- nagan Highlands fossil sites in Canada (49–51 Ma); L, Middle Eocene Kishenehn Formation in USA (46 Ma); M, Eocene Green River Formation in USA (48–51 Ma); N, Late Eocene Florissant For- mation in USA (34 Ma). Circles represent amber deposits, and squares mark rock fossil deposits. Eocene geographic map (approximately 50 Ma) was created by Blakey [34]. Current Biology Vol 24 No 14 1610

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