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An ammonite trapped in Burmese amber

An ammonite trapped in Burmese amber a,b,c,1 a,d,e,1 a,1 e f,g h i Tingting Yu , Richard Kelly , Lin Mu , Andrew Ross , Jim Kennedy , Pierre Broly , Fangyuan Xia , a,b a,b,j,2 k,2 Haichun Zhang , Bo Wang , and David Dilcher State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, b c China; CAS Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China; School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China; School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom; e f Department of Natural Sciences, National Museum of Scotland, Edinburgh EH1 1JF, United Kingdom; Oxford University Museum of Natural History, g h Oxford OX1 3PW, United Kingdom; Department of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom; Private address, 59840 i j Lompret, France; Lingpoge Amber Museum, Shanghai 201108, China; Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; and Department of Geology and Atmospheric Science, Indiana University, Bloomington, IN 47405 Contributed by David Dilcher, February 27, 2019 (sent for review December 13, 2018; reviewed by Phillip Barden and Enrique Peñalver Mollá) Amber is fossilized tree resin, and inclusions usually comprise (at least 40 individuals) of arthropods in this amber sample that live terrestrial and, rarely, aquatic organisms. Marine fossils are ex- today in both terrestrial and marine habitats. Of the terrestrial tremely rare in Cretaceous and Cenozoic ambers. Here, we report a fauna, Acari (mites) are the most abundant, with 23 specimens; also record of an ammonite with marine gastropods, intertidal isopods, present are Araneae (spiders), Diplopoda (millipedes), and repre- and diverse terrestrial arthropods as syninclusions in mid-Cretaceous sentatives of the insect orders Blattodea (cockroaches), Coleoptera Burmese amber. We used X-ray–microcomputed tomography (CT) to (beetles), Diptera (true flies), and Hymenoptera (wasps). The ar- obtain high-resolution 3D images of the ammonite, including its su- thropod assemblage consists mostly of forest floor-dwelling taxa, tures, which are diagnostically important for ammonites. The am- and living representatives are generally associated with leaf litter or monite is a juvenile Puzosia (Bhimaites) and provides supporting the top layers of soil. There are several isopods preserved which are evidence for a Late Albian–Early Cenomanian age of the amber. consistent with littoral or supralittoral taxa. In addition to the There is a diverse assemblage (at least 40 individuals) of arthropods ammonite itself, four definitively marine gastropod shells and one in this amber sample from both terrestrial and marine habitats, putatively marine isopod are present. including Isopoda, Acari (mites), Araneae (spiders), Diplopoda (millipedes), and representatives of the insect orders Blattodea Ammonite. The ammonite is a juvenile (the adapertural septa are (cockroaches), Coleoptera (beetles), Diptera (true flies), and Hyme- not crowded), has a maximum preserved diameter of 12 mm, and noptera (wasps). The incomplete preservation and lack of soft body appears to retain the original aragonitic shell, on the basis of its of the ammonite and marine gastropods suggest that they were appearance in reflected light (Fig. 2A). It is composed in part by dead and underwent abrasion on the seashore before entombment. the body chamber, but the apertural part is damaged, as revealed It is most likely that the resin fell to the beach from coastal trees, by the survival of a 60° sector of the umbilical wall extending picking up terrestrial arthropods and beach shells and, exceptionally, beyond the fragment of the inner flanks of the shell (Fig. 2). surviving the high-energy beach environment to be preserved as Coiling is moderately involute, with ∼64% of the previous whorl amber. Our findings not only represent a record of an ammonite in covered. The small, shallow umbilicus comprises 18% of the amber but also provide insights into the taphonomy of amber and diameter, the low umbilical wall is very weakly convex, and the the paleoecology of Cretaceous amber forests. umbilical shoulder is broadly rounded. The whorl section is amber ammonite fossil paleoecology taphonomy | | | | Significance mber provides a unique mode of preservation for organisms, Aquatic organisms are rarely found in amber, but when they Aand when inclusions are present they are usually 3D fossils occur they provide invaluable evidence for the better un- of terrestrial plants, microorganisms, arthropods, and even verte- derstanding of amber taphonomy and past ecosystems. We brate remains (1–3). Amber deposits are therefore considered to be report an ammonite and several marine gastropods alongside a exceptional Lagerstätten, providing unique windows into past eco- mixed assemblage of intertidal and terrestrial forest floor or- systems (4–6). Given that amber is formed by the fossilization of ganisms in mid-Cretaceous Burmese amber. Our discovery in- terrestrial plant resins, the capture of marine inclusions may be dicates that the Burmese amber forest was living near a considered extremely rare. However, some recent findings of ma- dynamic and shifting coastal environment. The ammonite also rine and freshwater fossils, particularly, microfossils such as dia- provides supporting evidence for the age of the amber, which toms, radiolarians, ostracods, and copepods, have provided fresh is still debated, and represents a rare example of dating using insights into amber taphonomy (7–12). fossils present inside the amber. Burmese amber (from northern Myanmar) contains the most diverse biota of all known Cretaceous ambers (13, 14). Over the Author contributions: B.W. and D.D. designed research; T.Y., R.K., L.M., A.R., J.K., and B.W. performed research; T.Y. and F.X. contributed new reagents/analytic tools; T.Y., R.K., last 100 years, and particularly in the past two decades, Burmese L.M., A.R., J.K., P.B., H.Z., B.W., and D.D. analyzed data; and T.Y., R.K., L.M., A.R., J.K., amber has received worldwide scientific interest; more than 500 B.W., and D.D. wrote the paper. families of invertebrates, vertebrates, protists, plants, and fungi Reviewers: P.B., New Jersey Institute of Technology; and E.P.M., Instituto Geológico y have been reported (15). Here, we provide an account of an Minero de España. exceptional piece of amber that preserves a unique assemblage The authors declare no conflict of interest. of marine macrofossils, alongside intertidal, fully terrestrial, and This open access article is distributed under Creative Commons Attribution License 4.0 possibly freshwater aquatic arthropods. (CC BY). T.Y., R.K., and L.M. contributed equally to this work. Results To whom correspondence may be addressed. Email: bowang@nigpas.ac.cn or dilcher@ The ammonite-bearing piece of amber (BA18100) was obtained indiana.edu. from an amber mine located near Noije Bum Village, Tanaing This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1821292116/-/DCSupplemental. Town (ref. 16 and Fig. 1). It is 33 mm long, 9.5 mm wide, and 29 mm high, and its weight is 6.08 g. There is a diverse assemblage Published online May 13, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1821292116 PNAS | June 4, 2019 | vol. 116 | no. 23 | 11345–11350 EVOLUTION Middle East, KwaZulu-Natal (South Africa), Mozambique, Madagascar, northern Pakistan, Australia, Patagonia, and Antarctica. There are similarities with juveniles of the Lower Albian Beudanticeras caseyi Collignon (ref. 19, p. 72, pl. 267, fig. 1165; holotype refigured by ref. 20, text-fig. 3j, k), known from Mada- gascar and northern KwaZulu-Natal (South Africa), and compara- bly sized juveniles of the Tunisian upper Lower Albian Beudanticeras dupinianum var. africana (ref. 21, p. 133, pl. 5, figs. 16, 17; text-fig. 49), as figured by Latil (ref. 22, pl. 3, figs. 1–19). These species, however, do not develop the low folds and undulations of the pre- sent specimen, and Beudanticeras is restricted to the Albian. Among the Puzosiinae, there are similarities with Puzosia (Bhimaites) Matsumoto (23), which ranges from the Upper Albian to the Upper Cenomanian and is known from western Europe, North Africa, Angola, KwaZulu-Natal (South Africa), Madagascar, South India, Japan, and Venezuela. The falcoid course of the ornament, which matches our specimen, is seen in several representatives of the genus, for example, the Upper Albian Puzosia (Bhimaites) pinguis (24) illustrated by Kennedy and Klinger (ref. 25, text-fig. 12a–g). A feature of Puzosia (Bhimaites) is the development of constrictions on the internal mold; their position is marked on the shell surface by much weaker depressions and associated collar ribs. These are very weakly expressed or absent in specimens com- parable in size to the present specimen [see, for example, the somewhat larger (30 mm diameter) individual of Bhimaites stoliczkai (26) figured by Renz (ref. 27, pl. 8, fig. 2)]; this species ranges from the Upper Albian to Lower Cenomanian. To conclude, features of the ammonite preserved most strongly suggest a juvenile Puzosia (Bhimaites), a subgenus that first appeared in the Upper Albian and ranged through the Cenomanian. Isopods. There are four isopod specimens in the amber (Fig. 3 A– C) and a further three specimens, which cannot be determined but may also be isopods. The first isopod (Fig. 3A) is consistent with terrestrial isopods in body shape: the eyes appear to be reduced, although this is not entirely clear, and there are six to Fig. 1. Geological and paleogeographic maps of Burmese amber. (A) Geo- seven pereonite segments with all pereopods ambulatory. The logical map showing the position of Burmese amber in Hukawng Valley, form of the uropods, if present, is not entirely clear, which is northern Myanmar. (B) Paleogeographic map showing the position (red unfortunate, as this is a key character for distinguishing marine triangle) of Burmese amber site during Late Albian (14, 17). and terrestrial taxa. It is similar to Armadillidae, which is recorded from Burmese amber (28), but also exhibits characters of marine taxa, such as having a larger posterior part, but many compressed, with a whorl breadth-to-height ratio of around 0.7 important characters are obscured, so it is difficult to identify (the specimen has undergone some postmortem deformation). with certainty. Although Armadillidae is generally considered to The inner flanks are very weakly convex, the outer flanks flat- be terrestrial, Poinar (28) considered that the features present in tened and weakly convergent, the ventrolateral shoulders broadly his fossil excluded it from those Oniscoidea mostly adapted to rounded, and the venter very weakly convex. Ornamentation con- terrestrial habitats, such as the strictly terrestrial Myanmariscus, sists of low falcoid folds, lirae, and riblets that are prorsiradiate and also recorded from Burmese amber (29). very weakly concave on the inner flank, flexing back and weakly Thesecondisopod(Fig. 3B) exhibits an elongated exopod uropod convex at midflank before flexing forward and weakly concave on and is similar to extant Sphaeromatidae in general habitus, indicating the outer flank, sweeping forward over the ventrolateral shoulders that it is possibly a marine or intertidal isopod. Sphaeromatids are and crossing the venter in a broad convexity. The suture of the typically marine, but many have been known to occur in estuaries penultimate whorl, revealed in X-ray–microcomputed tomography, (30) and intertidal zones and even to extend into freshwater habitats, is only partially decipherable. E/A is broad, bifid, and moderately including karstic streams and caves (31). The pale coloration and incised; A is narrower and possibly trifid; and A/U2 is narrow, little reduced eyes could indicate a stygobiont, but the color could also be incised, and bifid (Fig. 2B;see Movie S1 for detailed account). taphonomic. These characters are also not restricted to cave dwell- Given the age of the amber (discussed below), a compressed, ers, as some open-marine isopods also exhibit them (32). There is a involute, weakly ornamented ammonite could belong to one of three peculiar circular structure seemingly attached to this specimen (Fig. principal groups, the superfamilies Phylloceratoidea, Lytoceratoidea, 3D), although the association could be taphonomic. or Desmoceratoidea. The visible structure of the sutures and the The other two isopods (e.g., Fig. 3C) exhibit characters of lack of distinctive even lirae eliminate the first two superfamilies terrestrial or supralittoral isopods and are possibly associated from consideration. Within Desmoceratoidea, compressed weakly with the extant Oniscidea: Tylidae. The uropods appear to be ornamented taxa comparable to the present specimen occur in two reduced, as is typical of the more terrestrial taxa, and the visible subfamilies of the family Desmoceratidae, the Beudanticeratinae antennae are thick at the base with strong basal segments ta- and Puzosiinae. pering gradually toward the apex with a two- or three-jointed Among the Beudanticeratinae, a possible assignation is to flagellum. The first pair of antennae appear to be strongly re- Beudanticeras Hitzel (18), a genus that ranges from the Lower to duced, which is also an indication of the Oniscidea, with Tylidae Upper Albian and is known from Europe, North Africa, the only retaining the proximal article (33). 11346 | www.pnas.org/cgi/doi/10.1073/pnas.1821292116 Yu et al. Fig. 2. Ammonite Puzosia (Bhimaites) Matsumoto. (A) Lateral view under light microscopy. (B) Flattened sutures reconstructed by microtomography. (C) Microtomographic reconstruction, apparent view. (D) Microtomographic reconstruction, surface rendering; (E) Microtomographic reconstruction, virtual section. (Scale bars, 2 mm.) There are a few other specimens that are probably isopods, in- of Euphthiracaroidea (Fig. 5C), based on the fusion of the plates, cluding one that is badly damaged with most of its ventral side and some Brachypylina. obscured by a gastropod. The coloration and coxal plates are sim- Ptyctimous oribatids are common in soil/forest floor communities ilar to those of the specimen shown in Fig. 3A,but thereisapartial and are usually considered to be secondary decomposers/fungivores, eye preserved, and it is larger. It is closely associated with a gas- tropod, but this is probably taphonomic. There are two other very badly damaged specimens, which may be isopods and two others, which may be isopod larvae, but they are poorly preserved. Although taxonomic assignment is difficult based on speci- mens in which key characters cannot be observed, the specimens present in the piece of amber seem to be consistent with littoral or supralittoral isopods, with one possible fully marine species. Gastropods. Four marine gastropod shells are also preserved with the ammonite (Fig. 4), of which two are well-preserved and can be attributed to the genus Mathilda Semper (Mathildidae) by the small, conical shell with heterostrophic protoconchs, whorl sides rounded and basally subcarinate, base broadly arched, and or- nament of strong spiral cords and fine axial threads (34). Mathilda was mainly distributed in the western Tethys sea during the Cretaceous, and our fossils are a Cretaceous record of this genus from the eastern Tethys sea. Terrestrial Arthropod Assemblage. There are 22 oribatid mites in the piece, most of which are ptyctimous, meaning they can close their prodorsum over their legs as protection against predators (box mites). Most of the mites (15 individuals) are similar in appearance to Phthiracaridae (Fig. 5B), but the ventral shields would need to be examined to clarify this, which is difficult given Fig. 3. Isopods of uncertain taxonomic affinity, but generally consistent their position in the amber (Fig. 5A). They have previously only with littoral or supralittoral taxa. (A) Isopod 1. (B) Isopod 2. (C) Isopod 3. (D) been described from Baltic amber and younger deposits. Also, Circular structure attached to the dorsal surface of isopod 2. (Scale bars, although obscured in the piece, there appear to be representatives 1mm in A and C. Scale bar, 0.5 mm in B and D.) Yu et al. PNAS | June 4, 2019 | vol. 116 | no. 23 | 11347 EVOLUTION Fig. 4. Gastropods. (A) Mathilda sp. (B) Mathilda sp. (C) Undetermined specimen. (D) Undetermined specimen. (Scale bars, 1 mm.) although some ptyctimous mites are known to be xylophagous antennae, maxillary and labial palps, and the right fore, mid, and and feed on dead wood as primary decomposers (35). Either hind legs are preserved. There are no remains of the wings. The way, they are generally found in the presence of decaying plant maxillary palps are long; the head appears quite narrow, but not material (36, 37). Oribatids are generally free living in the upper entirely preserved. The partial preservation suggests that not all soil layers, but Phthiracaroidea are commonly found within of the cockroach became engulfed in the resin, and the exposed fallen leaves or conifer needles (37), and ground-dwelling species can be found up to 4 m from the ground on live tree trunks (38) with a clear gradient of community species composition as- cending the trunk (39). There is one spider preserved (Fig. 5D) that is unfortunately partly decomposed, and the eyes and chelicerae are not well preserved, so it is difficult to identify, but it is similar in general appearance to some Cretaceous Oonopidae which have been found in amber from Canada and Myanmar (40, 41). Oonopidae (goblin spiders) are described by Penney (40) as wandering, active predators, fast moving and nocturnal, and are known from a varied range of habitats (42), including the forest floor or tree bark (43). There are 12 adult insects preservedinthe piece, eightofwhich are true flies (Diptera), two are beetles (Coleoptera), one is a parasitic wasp (Hymenoptera), and one is a cockroach (Blattodea). There are also several larval specimens. Diptera is mostly repre- sented by small nematoceran midges or gnats (Ceratopogonidae, Cecidomyiidae, or Chironomidae), and there are two small bra- chyceran hump-backed flies with cyclorrhaphan-type antennae and wing venation (Fig. 5F) consistent with scuttleflies (Phoridae). Some nematoceran midges (e.g., chironomids) have aquatic larvae, which are usually found in freshwater habitats, but others (cerato- pogonids and cecidomyiids) could have terrestrial or plant gall stages. One of them may be a gall midge that could have been associated with trees, similar to the parasitoid wasp (Fig. 5G), which belongs to Chrysidoidea. There are two beetles preserved in the amber, but they are largely obscured by other material. The larger one (Fig. 5H)is obscured by a gastropod, but the characters that can be seen include hind and mid legs with the femur expanded; tibiae narrow at the base, expanding toward apex; thick tibial spines reaching at least the length of the first tarsomere; five-segmented tarsi, grad- ually reducing in length from the first to the fifth, with each expanding in width from base to apex; ring of clumped hairs around the apice of the tibiae and each tarsomere, except the fifth that has two claws; and fore leg curved in a raptorial style. The pronotum is transverse; the elytra are distorted but appear oval-shaped and may have a black-and-white–banded color pattern; the head (and antennae) are either not preserved or are obscured by Fig. 5. Amber inclusions. (A) Amber piece showing most large inclusions. (B) a gastropod shell. Acari: Phthiracaridae. (C) Acari: Euphthiracoidea. (D) Araneae: Oonopidae. The cockroach (Fig. 5I) is about 20 mm long, with most of the (E) Diplopoda. (F) Diptera: Phoridae. (G) Hymenoptera: Chrysidoidea. (H) head, thorax, and abdomen missing, but the general overall Coleoptera. (I) Blattodea. (Scale bar, 5 mm in A. Scale bars, 1 mm in E and H. shape is preserved. Also, many important characters, such as the Scale bars, 0.5 mm in B–D, F, and G. Scale bar, 2 mm in I.) 11348 | www.pnas.org/cgi/doi/10.1073/pnas.1821292116 Yu et al. parts decomposed before it was covered by another layer. Many possible scenarios: (i) There was a sandy beach with resin- cockroaches are found in forest floor, leaf litter habitats, and producing trees growing very close. The terrestrial insects were many are found associated with decaying wood, although others trapped in the resin while it was still on the tree, and as it are arboreal or aquatic (44). traveled down the tree trunk it picked up the lower-lying ter- One millipede is preserved (Fig. 5E) that is around 15 mm restrial arthropods, such as the mites. When it reached the long, very slender, and has relatively short legs. The amber ground (the beach?) it landed on the sand and shells, trapping around the millipede is cloudy, so it is difficult to observe characters the supralittoral isopods as they traversed the beach. As these in detail, certainly important characters such as the organ of forests are considered to have been coastal, this scenario could Tömösváry or ozopores. Millipedes are important detritivores and have been commonplace, but the probability of such amber are mainly forest floor dwellers and are considered to have been for pieces surviving would be slight, owing to the dynamic nature of their whole evolutionary history (45). The body form of the speci- beaches, which would explain the rarity of such pieces of amber men probably matches the “borer” (platydesmoid) type suggested in the fossil record. (ii) There was a tsunami that flooded the by Kime and Golovatch (46), which suggests that it inhabited the amber-producing forest, bringing marine debris into the forest leaf litter or uppermost soil layers (stratobiont) or that it was an and thus into contact with numerous blobs of resin. This would underbark xylobiont (47). certainly be an exceptional event, although it could possibly be expected that more diverse marine inclusions, including ones Discussion with soft-bodied preservation, would be found in the amber, if U-Pb dating of zircons from the volcanoclastic matrix of the this scenario were true. (iii) Being a tropical environment, it amber has given a maximum age of 98.8 ± 0.6 Ma (48), which could be assumed that tropical storms were fairly common and places it in the Early Cenomanian based on the 100.5 ± 0.4 Ma could therefore blow seashells and sand inland. This could also age assigned to the base of the stage by Cohen et al. (49); account for the martesine bivalve shells being found within the however, this dates the amber-bearing horizon, not the amber amber. However, if this was a fairly common event, it could be itself. This age is incompatible with the record of the exclusively expected that occurrences of marine shells in amber would be Upper Albian ammonite Mortoniceras, which was found in a more common as well. sandstone above primary Burmese amber deposits (16). The Marine and terrestrial organisms may get trapped in a single specimen of this ammonite was neither described nor figured, resin piece located at the edge of a coastal forest, and more and we could not examine it, as attempts to locate the specimen complicated scenarios such as liquid resin with sea water contact have not been successful; therefore we cannot confirm its iden- are not needed (6, 11, 54, 55), especially as Schmidt and Dilcher tity. Thus, the incompatibility of the age and the Mortoniceras (8) found that resin barely solidifies when submerged in water. ammonite remains unresolved. The presence of borings of The incomplete preservation and lack of the soft body of the martesine bivalves in the outer rim of pieces of Burmese amber marine ammonite (Fig. 2A) and four gastropods (Fig. 4) indicate suggested that the amber could be older than the age of the bed that they were dead and had experienced abrasion by the sea on it was collected from. Bivalves have also been found within the the seashore before they were engulfed by resin. Moreover, the amber and therefore bored into it while the amber was still soft aperture of the ammonite is filled with coarse shell sand, which is and are thus similar in age to the bed (50). also present in other parts of the amber piece (Fig. 5A), sug- Amber pieces can be reworked and redeposited in younger gesting that the resin-producing trees were very close to the deposits; therefore, dating amber is sometimes controversial. coast. Therefore, we consider that the first scenario is the most The amber-bearing strata can be dated from palynofloras, am- likely. Other marine inclusions in the future may suggest other monites, and radiodating evidence, but the amber could be older. scenarios, although it is possible for all of the scenarios above to Marine inclusions can help date ambers, as marine diatoms and have happened over the lifetime of the amber-producing forest. other marine microfossils supported an Albian–Cenomanian age It seems clear, however, that the forest was living near a dynamic of Charentese ambers of France (7, 51). The present discovery is and ever changing coastal environment. another interesting example of dating using fossils present inside the amber. Conclusions How did the amber that would have flowed from a tree cap- It is rare to find aquatic organisms in amber, and it is extremely ture both terrestrial (insects, millipedes, spiders, and mites) and rare to find marine organisms in amber, let alone macroscopic marine (ammonite, gastropods, and isopods) organisms? Anal- marine organisms mixed with intertidal, terrestrial, and poten- ysis of the depositional environment supports the model of an tially freshwater aquatic organisms. The exceptional occurrence estuarine, coastal landscape for the mid-Cretaceous amber for- of macroscopic marine macrofossils in the resin suggests that the ests. Poinar et al. (52) analyzed Burmese amber and found that amber forest was growing close to a coast, possibly next to a the most likely origin of the resin which formed the amber was beach, and could have been subjected to exceptional events. The araucarian conifers (but see ref. 53), which can be closely asso- shells may record an exceptionally high, perhaps storm- ciated with coastal habitats. Many pieces of Burmese amber were generated tide, or even a tsunami or other high-energy event. bored by martesine pholadid bivalves, indicating that the amber Alternatively, and more likely, the resin fell to the beach from was deposited in a brackish nearshore environment (50). Martesine coastal trees, picking up terrestrial arthropods and beach shells bivalves have also been found within the amber, indicating that and, exceptionally, surviving the high-energy beach environment the resin was still soft when the bivalves started boring into it, to be preserved as amber. which suggests that resin-producing trees were growing near to the site of deposition. The ammonite and gastropods had suffered Materials and Methods damage before entombment. For example, the ammonite had lost The amber piece (BA18100) is deposited in the Lingpoge Amber Museum in at least a 60° sector of its body chamber, indicating that this was Shanghai. Photographs were taken using a Zeiss AXIO Zoom.V16 microscope not the shell of a live individual. There is no evidence of any system at the State Key Laboratory of Paleobiology and Stratigraphy, soft-part preservation of any of the gastropods, which also suggests Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences that these were dead shells. The amber also contains some (NIGPAS). In most cases, incident and transmitted light were used simultaneously. shell sand. All images are digitally stacked photomicrographic composites of ∼40 indi- Of the many thousands of specimens of Burmese amber vidual focal planes that were obtained using the software Helicon Focus 6 studied, only one ammonite is known. It is an exceptional oc- (http://www.heliconsoft.com) for better illustration of the 3D structures, as currence and may record an exceptional event. There are three described by Schmidt et al. (56). Yu et al. PNAS | June 4, 2019 | vol. 116 | no. 23 | 11349 EVOLUTION To three-dimensionally reconstruct the ammonite, we scanned the fossil at VGStudio Max (version 3.0; Volume Graphics). The Nonplanar Clipping the micro-CT laboratory of NIGPAS, using a 3D X-ray microscope (3D-XRM), function program (VGStudio version 3.0) was used to reconstruct the suture Zeiss Xradia 520 versa. Unlike conventional micro-CT, which relies on maxi- along the curved surface of the ammonite. mum geometric magnification and a flat panel detector to achieve high resolution, 3D-XRM uses CCD-based objectives to achieve higher spatial ACKNOWLEDGMENTS. We are grateful to A. R. Schmidt and two reviewers resolution. Based on the size of the fossil specimen, a CCD-based 0.4× ob- for careful comments. Thanks to Z. Yin and S. Wu for the microcomputed jective was used, providing isotropic voxel sizes of 13.36 μm with the help of tomography reconstruction and to H. Pan, E. Sidorchuk, N. Bruce, and H. Matúš geometric magnification. During the scan, the acceleration voltage for the for assistance with identifications. This research was supported by the Second X-ray source was 70 kV (current 86 μA), and a thin filter (LE3) was used to Tibetan Plateau Scientific Expedition and Research (Grant 2019QZKK0706), avoid beam-hardening artifacts. To improve signal-to-noise ratio, 2001 Strategic Priority Research Program of the Chinese Academy of Sciences (Grants projections over 360° were collected, and the exposure time for each pro- XDB26000000 and XDA19050101), and National Natural Science Foundation of jection was 3 s. Volume data processing was performed using software China (Grants 41622201 and 41688103). 1. Martínez-Delclòs X, Briggs DEG, Peñalver E (2004) Taphonomy of insects in carbonates 29. Broly P, Maillet S, Ross AJ (2015) The first terrestrial isopod (Crustacea: Isopoda: and amber. Palaeogeogr Palaeoclimatol Palaeoecol 203:19–64. 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Survey of Natal and Zululand, ed Anderson W (Nabu Press, London), pp 161–250. 52. Poinar GO, Lambert JB, Wu Y (2007) Araucarian source of fossiliferous Burmese am- 25. Kennedy WJ, Klinger HC (2014) Cretaceous faunas from Zululand and Natal, South ber: Spectroscopic and anatomical evidence. J Bot Res Inst Tex 1:449–455. Africa. Valdedorsella, Pseudohaploceras, Puzosia, Bhimaites, Pachydesmoceras, Par- 53. Dutta S, Mallick M, Kumar K, Mann U, Greenwood PF (2011) Terpenoid composition apuzosia (Austiniceras), and P. (Parapuzosia) of the ammonite subfamily Puzosiinae and botanical affinity of Cretaceous resins from India and Myanmar. Int J Coal Geol Spath, 1922. Afr Nat Hist 10:1–46. 85:49–55. 26. Kossmat F (1898) Untersuchungen über die Sudindische Kreideformation. Beitr Pal- 54. Perrichot V (2004) Early Cretaceous amber from south-western France: Insight into äontol Osterreich-Ungarens Orients 11:89–152. the Mesozoic litter fauna. Geol Acta 2:9–22. 27. Renz O (1972) Die Gattungen Puzosia Bayle, Bhimaites Matsumoto und Desmoceras 55. Perrichot V, Girard V (2009) A unique piece of amber and the complexity of ancient Zittel (Ammonoidea) im Oberen Albien Venezuelas. Eclogae Geol Helv 65:701–724. forest ecosystems. Palaios 24:137–139. 28. Poinar GO (August 14, 2018) A new genus of terrestrial isopods (Crustacea: Oniscidea: 56. Schmidt AR, et al. (2010) Cretaceous African life captured in amber. Proc Natl Acad Sci Armadillidae) in Myanmar amber. Hist Biol, 10.1080/08912963.2018.1509964. USA 107:7329–7334. 11350 | www.pnas.org/cgi/doi/10.1073/pnas.1821292116 Yu et al. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Proceedings of the National Academy of Sciences of the United States of America Pubmed Central

An ammonite trapped in Burmese amber

Proceedings of the National Academy of Sciences of the United States of America , Volume 116 (23) – May 13, 2019

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Abstract

a,b,c,1 a,d,e,1 a,1 e f,g h i Tingting Yu , Richard Kelly , Lin Mu , Andrew Ross , Jim Kennedy , Pierre Broly , Fangyuan Xia , a,b a,b,j,2 k,2 Haichun Zhang , Bo Wang , and David Dilcher State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, b c China; CAS Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China; School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China; School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom; e f Department of Natural Sciences, National Museum of Scotland, Edinburgh EH1 1JF, United Kingdom; Oxford University Museum of Natural History, g h Oxford OX1 3PW, United Kingdom; Department of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom; Private address, 59840 i j Lompret, France; Lingpoge Amber Museum, Shanghai 201108, China; Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; and Department of Geology and Atmospheric Science, Indiana University, Bloomington, IN 47405 Contributed by David Dilcher, February 27, 2019 (sent for review December 13, 2018; reviewed by Phillip Barden and Enrique Peñalver Mollá) Amber is fossilized tree resin, and inclusions usually comprise (at least 40 individuals) of arthropods in this amber sample that live terrestrial and, rarely, aquatic organisms. Marine fossils are ex- today in both terrestrial and marine habitats. Of the terrestrial tremely rare in Cretaceous and Cenozoic ambers. Here, we report a fauna, Acari (mites) are the most abundant, with 23 specimens; also record of an ammonite with marine gastropods, intertidal isopods, present are Araneae (spiders), Diplopoda (millipedes), and repre- and diverse terrestrial arthropods as syninclusions in mid-Cretaceous sentatives of the insect orders Blattodea (cockroaches), Coleoptera Burmese amber. We used X-ray–microcomputed tomography (CT) to (beetles), Diptera (true flies), and Hymenoptera (wasps). The ar- obtain high-resolution 3D images of the ammonite, including its su- thropod assemblage consists mostly of forest floor-dwelling taxa, tures, which are diagnostically important for ammonites. The am- and living representatives are generally associated with leaf litter or monite is a juvenile Puzosia (Bhimaites) and provides supporting the top layers of soil. There are several isopods preserved which are evidence for a Late Albian–Early Cenomanian age of the amber. consistent with littoral or supralittoral taxa. In addition to the There is a diverse assemblage (at least 40 individuals) of arthropods ammonite itself, four definitively marine gastropod shells and one in this amber sample from both terrestrial and marine habitats, putatively marine isopod are present. including Isopoda, Acari (mites), Araneae (spiders), Diplopoda (millipedes), and representatives of the insect orders Blattodea Ammonite. The ammonite is a juvenile (the adapertural septa are (cockroaches), Coleoptera (beetles), Diptera (true flies), and Hyme- not crowded), has a maximum preserved diameter of 12 mm, and noptera (wasps). The incomplete preservation and lack of soft body appears to retain the original aragonitic shell, on the basis of its of the ammonite and marine gastropods suggest that they were appearance in reflected light (Fig. 2A). It is composed in part by dead and underwent abrasion on the seashore before entombment. the body chamber, but the apertural part is damaged, as revealed It is most likely that the resin fell to the beach from coastal trees, by the survival of a 60° sector of the umbilical wall extending picking up terrestrial arthropods and beach shells and, exceptionally, beyond the fragment of the inner flanks of the shell (Fig. 2). surviving the high-energy beach environment to be preserved as Coiling is moderately involute, with ∼64% of the previous whorl amber. Our findings not only represent a record of an ammonite in covered. The small, shallow umbilicus comprises 18% of the amber but also provide insights into the taphonomy of amber and diameter, the low umbilical wall is very weakly convex, and the the paleoecology of Cretaceous amber forests. umbilical shoulder is broadly rounded. The whorl section is amber ammonite fossil paleoecology taphonomy | | | | Significance mber provides a unique mode of preservation for organisms, Aquatic organisms are rarely found in amber, but when they Aand when inclusions are present they are usually 3D fossils occur they provide invaluable evidence for the better un- of terrestrial plants, microorganisms, arthropods, and even verte- derstanding of amber taphonomy and past ecosystems. We brate remains (1–3). Amber deposits are therefore considered to be report an ammonite and several marine gastropods alongside a exceptional Lagerstätten, providing unique windows into past eco- mixed assemblage of intertidal and terrestrial forest floor or- systems (4–6). Given that amber is formed by the fossilization of ganisms in mid-Cretaceous Burmese amber. Our discovery in- terrestrial plant resins, the capture of marine inclusions may be dicates that the Burmese amber forest was living near a considered extremely rare. However, some recent findings of ma- dynamic and shifting coastal environment. The ammonite also rine and freshwater fossils, particularly, microfossils such as dia- provides supporting evidence for the age of the amber, which toms, radiolarians, ostracods, and copepods, have provided fresh is still debated, and represents a rare example of dating using insights into amber taphonomy (7–12). fossils present inside the amber. Burmese amber (from northern Myanmar) contains the most diverse biota of all known Cretaceous ambers (13, 14). Over the Author contributions: B.W. and D.D. designed research; T.Y., R.K., L.M., A.R., J.K., and B.W. performed research; T.Y. and F.X. contributed new reagents/analytic tools; T.Y., R.K., last 100 years, and particularly in the past two decades, Burmese L.M., A.R., J.K., P.B., H.Z., B.W., and D.D. analyzed data; and T.Y., R.K., L.M., A.R., J.K., amber has received worldwide scientific interest; more than 500 B.W., and D.D. wrote the paper. families of invertebrates, vertebrates, protists, plants, and fungi Reviewers: P.B., New Jersey Institute of Technology; and E.P.M., Instituto Geológico y have been reported (15). Here, we provide an account of an Minero de España. exceptional piece of amber that preserves a unique assemblage The authors declare no conflict of interest. of marine macrofossils, alongside intertidal, fully terrestrial, and This open access article is distributed under Creative Commons Attribution License 4.0 possibly freshwater aquatic arthropods. (CC BY). T.Y., R.K., and L.M. contributed equally to this work. Results To whom correspondence may be addressed. Email: bowang@nigpas.ac.cn or dilcher@ The ammonite-bearing piece of amber (BA18100) was obtained indiana.edu. from an amber mine located near Noije Bum Village, Tanaing This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1821292116/-/DCSupplemental. Town (ref. 16 and Fig. 1). It is 33 mm long, 9.5 mm wide, and 29 mm high, and its weight is 6.08 g. There is a diverse assemblage Published online May 13, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1821292116 PNAS | June 4, 2019 | vol. 116 | no. 23 | 11345–11350 EVOLUTION Middle East, KwaZulu-Natal (South Africa), Mozambique, Madagascar, northern Pakistan, Australia, Patagonia, and Antarctica. There are similarities with juveniles of the Lower Albian Beudanticeras caseyi Collignon (ref. 19, p. 72, pl. 267, fig. 1165; holotype refigured by ref. 20, text-fig. 3j, k), known from Mada- gascar and northern KwaZulu-Natal (South Africa), and compara- bly sized juveniles of the Tunisian upper Lower Albian Beudanticeras dupinianum var. africana (ref. 21, p. 133, pl. 5, figs. 16, 17; text-fig. 49), as figured by Latil (ref. 22, pl. 3, figs. 1–19). These species, however, do not develop the low folds and undulations of the pre- sent specimen, and Beudanticeras is restricted to the Albian. Among the Puzosiinae, there are similarities with Puzosia (Bhimaites) Matsumoto (23), which ranges from the Upper Albian to the Upper Cenomanian and is known from western Europe, North Africa, Angola, KwaZulu-Natal (South Africa), Madagascar, South India, Japan, and Venezuela. The falcoid course of the ornament, which matches our specimen, is seen in several representatives of the genus, for example, the Upper Albian Puzosia (Bhimaites) pinguis (24) illustrated by Kennedy and Klinger (ref. 25, text-fig. 12a–g). A feature of Puzosia (Bhimaites) is the development of constrictions on the internal mold; their position is marked on the shell surface by much weaker depressions and associated collar ribs. These are very weakly expressed or absent in specimens com- parable in size to the present specimen [see, for example, the somewhat larger (30 mm diameter) individual of Bhimaites stoliczkai (26) figured by Renz (ref. 27, pl. 8, fig. 2)]; this species ranges from the Upper Albian to Lower Cenomanian. To conclude, features of the ammonite preserved most strongly suggest a juvenile Puzosia (Bhimaites), a subgenus that first appeared in the Upper Albian and ranged through the Cenomanian. Isopods. There are four isopod specimens in the amber (Fig. 3 A– C) and a further three specimens, which cannot be determined but may also be isopods. The first isopod (Fig. 3A) is consistent with terrestrial isopods in body shape: the eyes appear to be reduced, although this is not entirely clear, and there are six to Fig. 1. Geological and paleogeographic maps of Burmese amber. (A) Geo- seven pereonite segments with all pereopods ambulatory. The logical map showing the position of Burmese amber in Hukawng Valley, form of the uropods, if present, is not entirely clear, which is northern Myanmar. (B) Paleogeographic map showing the position (red unfortunate, as this is a key character for distinguishing marine triangle) of Burmese amber site during Late Albian (14, 17). and terrestrial taxa. It is similar to Armadillidae, which is recorded from Burmese amber (28), but also exhibits characters of marine taxa, such as having a larger posterior part, but many compressed, with a whorl breadth-to-height ratio of around 0.7 important characters are obscured, so it is difficult to identify (the specimen has undergone some postmortem deformation). with certainty. Although Armadillidae is generally considered to The inner flanks are very weakly convex, the outer flanks flat- be terrestrial, Poinar (28) considered that the features present in tened and weakly convergent, the ventrolateral shoulders broadly his fossil excluded it from those Oniscoidea mostly adapted to rounded, and the venter very weakly convex. Ornamentation con- terrestrial habitats, such as the strictly terrestrial Myanmariscus, sists of low falcoid folds, lirae, and riblets that are prorsiradiate and also recorded from Burmese amber (29). very weakly concave on the inner flank, flexing back and weakly Thesecondisopod(Fig. 3B) exhibits an elongated exopod uropod convex at midflank before flexing forward and weakly concave on and is similar to extant Sphaeromatidae in general habitus, indicating the outer flank, sweeping forward over the ventrolateral shoulders that it is possibly a marine or intertidal isopod. Sphaeromatids are and crossing the venter in a broad convexity. The suture of the typically marine, but many have been known to occur in estuaries penultimate whorl, revealed in X-ray–microcomputed tomography, (30) and intertidal zones and even to extend into freshwater habitats, is only partially decipherable. E/A is broad, bifid, and moderately including karstic streams and caves (31). The pale coloration and incised; A is narrower and possibly trifid; and A/U2 is narrow, little reduced eyes could indicate a stygobiont, but the color could also be incised, and bifid (Fig. 2B;see Movie S1 for detailed account). taphonomic. These characters are also not restricted to cave dwell- Given the age of the amber (discussed below), a compressed, ers, as some open-marine isopods also exhibit them (32). There is a involute, weakly ornamented ammonite could belong to one of three peculiar circular structure seemingly attached to this specimen (Fig. principal groups, the superfamilies Phylloceratoidea, Lytoceratoidea, 3D), although the association could be taphonomic. or Desmoceratoidea. The visible structure of the sutures and the The other two isopods (e.g., Fig. 3C) exhibit characters of lack of distinctive even lirae eliminate the first two superfamilies terrestrial or supralittoral isopods and are possibly associated from consideration. Within Desmoceratoidea, compressed weakly with the extant Oniscidea: Tylidae. The uropods appear to be ornamented taxa comparable to the present specimen occur in two reduced, as is typical of the more terrestrial taxa, and the visible subfamilies of the family Desmoceratidae, the Beudanticeratinae antennae are thick at the base with strong basal segments ta- and Puzosiinae. pering gradually toward the apex with a two- or three-jointed Among the Beudanticeratinae, a possible assignation is to flagellum. The first pair of antennae appear to be strongly re- Beudanticeras Hitzel (18), a genus that ranges from the Lower to duced, which is also an indication of the Oniscidea, with Tylidae Upper Albian and is known from Europe, North Africa, the only retaining the proximal article (33). 11346 | www.pnas.org/cgi/doi/10.1073/pnas.1821292116 Yu et al. Fig. 2. Ammonite Puzosia (Bhimaites) Matsumoto. (A) Lateral view under light microscopy. (B) Flattened sutures reconstructed by microtomography. (C) Microtomographic reconstruction, apparent view. (D) Microtomographic reconstruction, surface rendering; (E) Microtomographic reconstruction, virtual section. (Scale bars, 2 mm.) There are a few other specimens that are probably isopods, in- of Euphthiracaroidea (Fig. 5C), based on the fusion of the plates, cluding one that is badly damaged with most of its ventral side and some Brachypylina. obscured by a gastropod. The coloration and coxal plates are sim- Ptyctimous oribatids are common in soil/forest floor communities ilar to those of the specimen shown in Fig. 3A,but thereisapartial and are usually considered to be secondary decomposers/fungivores, eye preserved, and it is larger. It is closely associated with a gas- tropod, but this is probably taphonomic. There are two other very badly damaged specimens, which may be isopods and two others, which may be isopod larvae, but they are poorly preserved. Although taxonomic assignment is difficult based on speci- mens in which key characters cannot be observed, the specimens present in the piece of amber seem to be consistent with littoral or supralittoral isopods, with one possible fully marine species. Gastropods. Four marine gastropod shells are also preserved with the ammonite (Fig. 4), of which two are well-preserved and can be attributed to the genus Mathilda Semper (Mathildidae) by the small, conical shell with heterostrophic protoconchs, whorl sides rounded and basally subcarinate, base broadly arched, and or- nament of strong spiral cords and fine axial threads (34). Mathilda was mainly distributed in the western Tethys sea during the Cretaceous, and our fossils are a Cretaceous record of this genus from the eastern Tethys sea. Terrestrial Arthropod Assemblage. There are 22 oribatid mites in the piece, most of which are ptyctimous, meaning they can close their prodorsum over their legs as protection against predators (box mites). Most of the mites (15 individuals) are similar in appearance to Phthiracaridae (Fig. 5B), but the ventral shields would need to be examined to clarify this, which is difficult given Fig. 3. Isopods of uncertain taxonomic affinity, but generally consistent their position in the amber (Fig. 5A). They have previously only with littoral or supralittoral taxa. (A) Isopod 1. (B) Isopod 2. (C) Isopod 3. (D) been described from Baltic amber and younger deposits. Also, Circular structure attached to the dorsal surface of isopod 2. (Scale bars, although obscured in the piece, there appear to be representatives 1mm in A and C. Scale bar, 0.5 mm in B and D.) Yu et al. PNAS | June 4, 2019 | vol. 116 | no. 23 | 11347 EVOLUTION Fig. 4. Gastropods. (A) Mathilda sp. (B) Mathilda sp. (C) Undetermined specimen. (D) Undetermined specimen. (Scale bars, 1 mm.) although some ptyctimous mites are known to be xylophagous antennae, maxillary and labial palps, and the right fore, mid, and and feed on dead wood as primary decomposers (35). Either hind legs are preserved. There are no remains of the wings. The way, they are generally found in the presence of decaying plant maxillary palps are long; the head appears quite narrow, but not material (36, 37). Oribatids are generally free living in the upper entirely preserved. The partial preservation suggests that not all soil layers, but Phthiracaroidea are commonly found within of the cockroach became engulfed in the resin, and the exposed fallen leaves or conifer needles (37), and ground-dwelling species can be found up to 4 m from the ground on live tree trunks (38) with a clear gradient of community species composition as- cending the trunk (39). There is one spider preserved (Fig. 5D) that is unfortunately partly decomposed, and the eyes and chelicerae are not well preserved, so it is difficult to identify, but it is similar in general appearance to some Cretaceous Oonopidae which have been found in amber from Canada and Myanmar (40, 41). Oonopidae (goblin spiders) are described by Penney (40) as wandering, active predators, fast moving and nocturnal, and are known from a varied range of habitats (42), including the forest floor or tree bark (43). There are 12 adult insects preservedinthe piece, eightofwhich are true flies (Diptera), two are beetles (Coleoptera), one is a parasitic wasp (Hymenoptera), and one is a cockroach (Blattodea). There are also several larval specimens. Diptera is mostly repre- sented by small nematoceran midges or gnats (Ceratopogonidae, Cecidomyiidae, or Chironomidae), and there are two small bra- chyceran hump-backed flies with cyclorrhaphan-type antennae and wing venation (Fig. 5F) consistent with scuttleflies (Phoridae). Some nematoceran midges (e.g., chironomids) have aquatic larvae, which are usually found in freshwater habitats, but others (cerato- pogonids and cecidomyiids) could have terrestrial or plant gall stages. One of them may be a gall midge that could have been associated with trees, similar to the parasitoid wasp (Fig. 5G), which belongs to Chrysidoidea. There are two beetles preserved in the amber, but they are largely obscured by other material. The larger one (Fig. 5H)is obscured by a gastropod, but the characters that can be seen include hind and mid legs with the femur expanded; tibiae narrow at the base, expanding toward apex; thick tibial spines reaching at least the length of the first tarsomere; five-segmented tarsi, grad- ually reducing in length from the first to the fifth, with each expanding in width from base to apex; ring of clumped hairs around the apice of the tibiae and each tarsomere, except the fifth that has two claws; and fore leg curved in a raptorial style. The pronotum is transverse; the elytra are distorted but appear oval-shaped and may have a black-and-white–banded color pattern; the head (and antennae) are either not preserved or are obscured by Fig. 5. Amber inclusions. (A) Amber piece showing most large inclusions. (B) a gastropod shell. Acari: Phthiracaridae. (C) Acari: Euphthiracoidea. (D) Araneae: Oonopidae. The cockroach (Fig. 5I) is about 20 mm long, with most of the (E) Diplopoda. (F) Diptera: Phoridae. (G) Hymenoptera: Chrysidoidea. (H) head, thorax, and abdomen missing, but the general overall Coleoptera. (I) Blattodea. (Scale bar, 5 mm in A. Scale bars, 1 mm in E and H. shape is preserved. Also, many important characters, such as the Scale bars, 0.5 mm in B–D, F, and G. Scale bar, 2 mm in I.) 11348 | www.pnas.org/cgi/doi/10.1073/pnas.1821292116 Yu et al. parts decomposed before it was covered by another layer. Many possible scenarios: (i) There was a sandy beach with resin- cockroaches are found in forest floor, leaf litter habitats, and producing trees growing very close. The terrestrial insects were many are found associated with decaying wood, although others trapped in the resin while it was still on the tree, and as it are arboreal or aquatic (44). traveled down the tree trunk it picked up the lower-lying ter- One millipede is preserved (Fig. 5E) that is around 15 mm restrial arthropods, such as the mites. When it reached the long, very slender, and has relatively short legs. The amber ground (the beach?) it landed on the sand and shells, trapping around the millipede is cloudy, so it is difficult to observe characters the supralittoral isopods as they traversed the beach. As these in detail, certainly important characters such as the organ of forests are considered to have been coastal, this scenario could Tömösváry or ozopores. Millipedes are important detritivores and have been commonplace, but the probability of such amber are mainly forest floor dwellers and are considered to have been for pieces surviving would be slight, owing to the dynamic nature of their whole evolutionary history (45). The body form of the speci- beaches, which would explain the rarity of such pieces of amber men probably matches the “borer” (platydesmoid) type suggested in the fossil record. (ii) There was a tsunami that flooded the by Kime and Golovatch (46), which suggests that it inhabited the amber-producing forest, bringing marine debris into the forest leaf litter or uppermost soil layers (stratobiont) or that it was an and thus into contact with numerous blobs of resin. This would underbark xylobiont (47). certainly be an exceptional event, although it could possibly be expected that more diverse marine inclusions, including ones Discussion with soft-bodied preservation, would be found in the amber, if U-Pb dating of zircons from the volcanoclastic matrix of the this scenario were true. (iii) Being a tropical environment, it amber has given a maximum age of 98.8 ± 0.6 Ma (48), which could be assumed that tropical storms were fairly common and places it in the Early Cenomanian based on the 100.5 ± 0.4 Ma could therefore blow seashells and sand inland. This could also age assigned to the base of the stage by Cohen et al. (49); account for the martesine bivalve shells being found within the however, this dates the amber-bearing horizon, not the amber amber. However, if this was a fairly common event, it could be itself. This age is incompatible with the record of the exclusively expected that occurrences of marine shells in amber would be Upper Albian ammonite Mortoniceras, which was found in a more common as well. sandstone above primary Burmese amber deposits (16). The Marine and terrestrial organisms may get trapped in a single specimen of this ammonite was neither described nor figured, resin piece located at the edge of a coastal forest, and more and we could not examine it, as attempts to locate the specimen complicated scenarios such as liquid resin with sea water contact have not been successful; therefore we cannot confirm its iden- are not needed (6, 11, 54, 55), especially as Schmidt and Dilcher tity. Thus, the incompatibility of the age and the Mortoniceras (8) found that resin barely solidifies when submerged in water. ammonite remains unresolved. The presence of borings of The incomplete preservation and lack of the soft body of the martesine bivalves in the outer rim of pieces of Burmese amber marine ammonite (Fig. 2A) and four gastropods (Fig. 4) indicate suggested that the amber could be older than the age of the bed that they were dead and had experienced abrasion by the sea on it was collected from. Bivalves have also been found within the the seashore before they were engulfed by resin. Moreover, the amber and therefore bored into it while the amber was still soft aperture of the ammonite is filled with coarse shell sand, which is and are thus similar in age to the bed (50). also present in other parts of the amber piece (Fig. 5A), sug- Amber pieces can be reworked and redeposited in younger gesting that the resin-producing trees were very close to the deposits; therefore, dating amber is sometimes controversial. coast. Therefore, we consider that the first scenario is the most The amber-bearing strata can be dated from palynofloras, am- likely. Other marine inclusions in the future may suggest other monites, and radiodating evidence, but the amber could be older. scenarios, although it is possible for all of the scenarios above to Marine inclusions can help date ambers, as marine diatoms and have happened over the lifetime of the amber-producing forest. other marine microfossils supported an Albian–Cenomanian age It seems clear, however, that the forest was living near a dynamic of Charentese ambers of France (7, 51). The present discovery is and ever changing coastal environment. another interesting example of dating using fossils present inside the amber. Conclusions How did the amber that would have flowed from a tree cap- It is rare to find aquatic organisms in amber, and it is extremely ture both terrestrial (insects, millipedes, spiders, and mites) and rare to find marine organisms in amber, let alone macroscopic marine (ammonite, gastropods, and isopods) organisms? Anal- marine organisms mixed with intertidal, terrestrial, and poten- ysis of the depositional environment supports the model of an tially freshwater aquatic organisms. The exceptional occurrence estuarine, coastal landscape for the mid-Cretaceous amber for- of macroscopic marine macrofossils in the resin suggests that the ests. Poinar et al. (52) analyzed Burmese amber and found that amber forest was growing close to a coast, possibly next to a the most likely origin of the resin which formed the amber was beach, and could have been subjected to exceptional events. The araucarian conifers (but see ref. 53), which can be closely asso- shells may record an exceptionally high, perhaps storm- ciated with coastal habitats. Many pieces of Burmese amber were generated tide, or even a tsunami or other high-energy event. bored by martesine pholadid bivalves, indicating that the amber Alternatively, and more likely, the resin fell to the beach from was deposited in a brackish nearshore environment (50). Martesine coastal trees, picking up terrestrial arthropods and beach shells bivalves have also been found within the amber, indicating that and, exceptionally, surviving the high-energy beach environment the resin was still soft when the bivalves started boring into it, to be preserved as amber. which suggests that resin-producing trees were growing near to the site of deposition. The ammonite and gastropods had suffered Materials and Methods damage before entombment. For example, the ammonite had lost The amber piece (BA18100) is deposited in the Lingpoge Amber Museum in at least a 60° sector of its body chamber, indicating that this was Shanghai. Photographs were taken using a Zeiss AXIO Zoom.V16 microscope not the shell of a live individual. There is no evidence of any system at the State Key Laboratory of Paleobiology and Stratigraphy, soft-part preservation of any of the gastropods, which also suggests Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences that these were dead shells. The amber also contains some (NIGPAS). In most cases, incident and transmitted light were used simultaneously. shell sand. All images are digitally stacked photomicrographic composites of ∼40 indi- Of the many thousands of specimens of Burmese amber vidual focal planes that were obtained using the software Helicon Focus 6 studied, only one ammonite is known. It is an exceptional oc- (http://www.heliconsoft.com) for better illustration of the 3D structures, as currence and may record an exceptional event. There are three described by Schmidt et al. (56). Yu et al. PNAS | June 4, 2019 | vol. 116 | no. 23 | 11349 EVOLUTION To three-dimensionally reconstruct the ammonite, we scanned the fossil at VGStudio Max (version 3.0; Volume Graphics). The Nonplanar Clipping the micro-CT laboratory of NIGPAS, using a 3D X-ray microscope (3D-XRM), function program (VGStudio version 3.0) was used to reconstruct the suture Zeiss Xradia 520 versa. Unlike conventional micro-CT, which relies on maxi- along the curved surface of the ammonite. mum geometric magnification and a flat panel detector to achieve high resolution, 3D-XRM uses CCD-based objectives to achieve higher spatial ACKNOWLEDGMENTS. We are grateful to A. R. Schmidt and two reviewers resolution. Based on the size of the fossil specimen, a CCD-based 0.4× ob- for careful comments. Thanks to Z. Yin and S. Wu for the microcomputed jective was used, providing isotropic voxel sizes of 13.36 μm with the help of tomography reconstruction and to H. Pan, E. Sidorchuk, N. Bruce, and H. Matúš geometric magnification. During the scan, the acceleration voltage for the for assistance with identifications. This research was supported by the Second X-ray source was 70 kV (current 86 μA), and a thin filter (LE3) was used to Tibetan Plateau Scientific Expedition and Research (Grant 2019QZKK0706), avoid beam-hardening artifacts. To improve signal-to-noise ratio, 2001 Strategic Priority Research Program of the Chinese Academy of Sciences (Grants projections over 360° were collected, and the exposure time for each pro- XDB26000000 and XDA19050101), and National Natural Science Foundation of jection was 3 s. Volume data processing was performed using software China (Grants 41622201 and 41688103). 1. Martínez-Delclòs X, Briggs DEG, Peñalver E (2004) Taphonomy of insects in carbonates 29. Broly P, Maillet S, Ross AJ (2015) The first terrestrial isopod (Crustacea: Isopoda: and amber. Palaeogeogr Palaeoclimatol Palaeoecol 203:19–64. 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