Unlocking preservation bias in the amber insect fossil record through experimental decay

McCoy, Victoria E.; Soriano, Carmen; Pegoraro, Mirko; Luo, Ting; Boom, Arnoud; Foxman, Betsy; Gabbott, Sarah E.

doi:10.1371/journal.pone.0195482

Title: Unlocking preservation bias in the amber insect fossil record through experimental decay

Journal Article · 05 April 2018 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0195482 · OSTI ID:1473585

^[1]; Soriano, Carmen ^[2]; Pegoraro, Mirko ^[3]; Luo, Ting ^[4]; Boom, Arnoud ^[5]; Foxman, Betsy ^[4]; Gabbott, Sarah E. ^[5]

Univ. of Leicester (United Kingdom); Univ. of Bonn (Germany)
Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Leicester (United Kingdom); John Moores Univ., Liverpool (United Kingdom)
Univ. of Michigan, Ann Arbor, MI (United States)
Univ. of Leicester (United Kingdom)

Fossils entombed in amber are a unique resource for reconstructing forest ecosystems, and resolving relationships of modern taxa. Such fossils are famous for their perfect, life-like appearance. However, preservation quality is vast with many sites showing only cuticular preservation, or no fossils. The taphonomic processes that control this range are largely unknown; as such, we know little about potential bias in this important record. Here we employ actualistic experiments, using, fruit flies and modern tree resin to determine whether resin type, gut microbiota, and dehydration prior to entombment affects decay. We used solid phase microextraction gas chromatography-mass spectrometry (SPME GC-MS) to confirm distinct tree resin chemistry; gut microbiota of flies was modified using antibiotics and categorized though sequencing. Decay was assessed using phase contrast synchrotron tomography. Resin type demonstrates a significant control on decay rate. The composition of the gut microbiota was also influential, with minor changes in composition affecting decay rate. Dehydration prior to entombment, contrary to expectations, enhanced decay. Our analyses show that there is potential significant bias in the amber fossil record, especially between sites with different resin types where ecological completeness and preservational fidelity are likely affected.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1473585

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 4 Vol. 13; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Chemical Signatures of Fossilized Resins and Recent Plant Exudates Lambert, Joseph B.; Santiago-Blay, Jorge A.; Anderson, Ken B. Angewandte Chemie International Edition, Vol. 47, Issue 50 https://doi.org/10.1002/anie.200705973	journal	December 2008
Headspace solid phase microextraction for screening for the presence of resins in Egyptian archaeological samples Hamm, Sandrine; Bleton, Jean; Tchapla, Alain Journal of Separation Science, Vol. 27, Issue 3 https://doi.org/10.1002/jssc.200301611	journal	February 2004
Optimization of headspace solid phase microextraction for gas chromatography/mass spectrometry analysis of widely different volatility and polarity terpenoids in olibanum Hamm, Sandrine; Lesellier, Eric; Bleton, Jean Journal of Chromatography A, Vol. 1018, Issue 1 https://doi.org/10.1016/j.chroma.2003.08.027	journal	November 2003
Transient adult microbiota, gut homeostasis and longevity: Novel insights from the Drosophila model Erkosar, Berra; Leulier, François FEBS Letters, Vol. 588, Issue 22 https://doi.org/10.1016/j.febslet.2014.06.041	journal	June 2014
A chemical investigation by headspace SPME and GC–MS of volatile and semi-volatile terpenes in various olibanum samples Hamm, Sandrine; Bleton, Jean; Connan, Jacques Phytochemistry, Vol. 66, Issue 12 https://doi.org/10.1016/j.phytochem.2005.04.025	journal	June 2005
Taxonomic trends in the resolution of detail preserved in fossil phosphatized soft tissues Wilby, Philip R.; Briggs, Derek E. G. Geobios, Vol. 30 https://doi.org/10.1016/s0016-6995(97)80056-3	journal	January 1997
Taxonomic and Chemical Relationships Revealed by Nuclear Magnetic Resonance Spectra of Plant Exudates Lambert, Joseph B.; Wu, Yuyang; Santiago-Blay, Jorge A. Journal of Natural Products, Vol. 68, Issue 5 https://doi.org/10.1021/np050005f	journal	May 2005
Antimicrobial agents from plants: antibacterial activity of plant volatile oils Dorman, H. J. D.; Deans, S. G. Journal of Applied Microbiology, Vol. 88, Issue 2 https://doi.org/10.1046/j.1365-2672.2000.00969.x	journal	February 2000
Preservative qualities of recent and fossil resins: Electron micrograph studies on tissue preserved in Baltic amber Poinar, George O.; Hess, Roberta Journal of Baltic Studies, Vol. 16, Issue 3 https://doi.org/10.1080/01629778500000141	journal	September 1985
Fossil fish stomachs: A microenvironment for exceptional preservation Wilby, Philip R.; Martill, David M. Historical Biology, Vol. 6, Issue 1 https://doi.org/10.1080/10292389209380416	journal	January 1992
Comparing amber fossil assemblages across the Cenozoic Penney, David; Langan, A. Mark Biology Letters, Vol. 2, Issue 2 https://doi.org/10.1098/rsbl.2006.0442	journal	December 2005
Chemical preservation of plants and insects in natural resins Stankiewicz, B. A.; Poinar, H. N.; Briggs, D. E. G. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 265, Issue 1397 https://doi.org/10.1098/rspb.1998.0342	journal	April 1998
Wolbachia and Virus Protection in Insects Hedges, L. M.; Brownlie, J. C.; O'Neill, S. L. Science, Vol. 322, Issue 5902 https://doi.org/10.1126/science.1162418	journal	October 2008
Ultrastructure of 40-Million-Year-Old Insect Tissue Poinar, G. O.; Hess, R. Science, Vol. 215, Issue 4537 https://doi.org/10.1126/science.215.4537.1241	journal	March 1982
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities Lozupone, C.; Knight, R. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/aem.71.12.8228-8235.2005	journal	December 2005
Microbiota-Induced Changes in Drosophila melanogaster Host Gene Expression and Gut Morphology Broderick, Nichole A.; Buchon, Nicolas; Lemaitre, Bruno mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mbio.01117-14	journal	July 2014
The First Ant-Termite Syninclusion in Amber with CT-Scan Analysis of Taphonomy Coty, David; Aria, Cédric; Garrouste, Romain PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104410	journal	August 2014
Entrapment Bias of Arthropods in Miocene Amber Revealed by Trapping Experiments in a Tropical Forest in Chiapas, Mexico Solórzano Kraemer, Mónica M.; Kraemer, Atahualpa S.; Stebner, Frauke PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0118820	journal	March 2015
Exceptional Preservation of Dipteran Flight Muscle and the Taphonomy of Insects in Amber Henwood, Alison PALAIOS, Vol. 7, Issue 2 https://doi.org/10.2307/3514931	journal	April 1992
Distribution de la flore alpine dans le Bassin des Dranses et dans quelques régions voisines Paul, Jaccard, Imprimerie Corbaz & Comp. https://doi.org/10.5169/seals-266440	text	January 1901
Chemical Signatures of Fossilized Resins and Recent Plant Exudates Lambert, Joseph B.; Santiago-Blay, Jorge A.; Anderson, Ken B. Angewandte Chemie International Edition, Vol. 47, Issue 50 https://doi.org/10.1002/anie.200705973	journal	December 2008
Antimicrobial activity of essential oils from Tunisian aromatic plants Bouzouita, Nabiha; Kachouri, Faten; Hamdi, Moktar Flavour and Fragrance Journal, Vol. 18, Issue 5 https://doi.org/10.1002/ffj.1200	journal	January 2003
A Mathematical Theory of Communication Shannon, C. E. Bell System Technical Journal, Vol. 27, Issue 4 https://doi.org/10.1002/j.1538-7305.1948.tb00917.x	journal	October 1948
A Mathematical Theory of Communication Shannon, C. E. Bell System Technical Journal, Vol. 27, Issue 3 https://doi.org/10.1002/j.1538-7305.1948.tb01338.x	journal	July 1948
Headspace solid phase microextraction for screening for the presence of resins in Egyptian archaeological samples Hamm, Sandrine; Bleton, Jean; Tchapla, Alain Journal of Separation Science, Vol. 27, Issue 3 https://doi.org/10.1002/jssc.200301611	journal	February 2004
Examination of amber and related materials by NMR spectroscopy: NMR of amber Lambert, Joseph B.; Santiago-Blay, Jorge A.; Wu, Yuyang Magnetic Resonance in Chemistry, Vol. 53, Issue 1 https://doi.org/10.1002/mrc.4121	journal	August 2014
Taxonomic trends in the resolution of detail preserved in fossil phosphatized soft tissues Wilby, Philip R.; Briggs, Derek E. G. Geobios, Vol. 30 https://doi.org/10.1016/S0016-6995(97)80056-3	journal	January 1997
Taphonomy of insects in carbonates and amber Martı́nez-Delclòs, Xavier; Briggs, Derek E. G.; Peñalver, Enrique Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 203, Issue 1-2 https://doi.org/10.1016/S0031-0182(03)00643-6	journal	January 2004
Optimization of headspace solid phase microextraction for gas chromatography/mass spectrometry analysis of widely different volatility and polarity terpenoids in olibanum Hamm, Sandrine; Lesellier, Eric; Bleton, Jean Journal of Chromatography A, Vol. 1018, Issue 1 https://doi.org/10.1016/j.chroma.2003.08.027	journal	November 2003
Fossiliferous amber deposits from the Cretaceous (Albian) of Spain Delclòs, Xavier; Arillo, Antonio; Peñalver, Enrique Comptes Rendus Palevol, Vol. 6, Issue 1-2 https://doi.org/10.1016/j.crpv.2006.09.003	journal	January 2007
Synchrotron X-ray imaging of inclusions in amber Soriano, Carmen; Archer, Mike; Azar, Dany Comptes Rendus Palevol, Vol. 9, Issue 6-7 https://doi.org/10.1016/j.crpv.2010.07.014	journal	September 2010
Transient adult microbiota, gut homeostasis and longevity: Novel insights from the Drosophila model Erkosar, Berra; Leulier, François FEBS Letters, Vol. 588, Issue 22 https://doi.org/10.1016/j.febslet.2014.06.041	journal	June 2014
Molecular composition and chemotaxonomic aspects of Eocene amber from the Ameki Formation, Nigeria Sonibare, Oluwadayo O.; Hoffmann, Thorsten; Foley, Stephen F. Organic Geochemistry, Vol. 51 https://doi.org/10.1016/j.orggeochem.2012.08.003	journal	October 2012
Importance of Dominican Republic amber for determining taxonomic bias of fossil resin preservation—A case study of spiders Penney, David Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 223, Issue 1-2 https://doi.org/10.1016/j.palaeo.2005.03.022	journal	July 2005
A chemical investigation by headspace SPME and GC–MS of volatile and semi-volatile terpenes in various olibanum samples Hamm, Sandrine; Bleton, Jean; Connan, Jacques Phytochemistry, Vol. 66, Issue 12 https://doi.org/10.1016/j.phytochem.2005.04.025	journal	June 2005
Amber Labandeira, Conrad C. The Paleontological Society Papers, Vol. 20 https://doi.org/10.1017/S1089332600002850	journal	October 2014
Amber: the Organic Gemstone Lambert, Joseph B.; Poinar, George O. Accounts of Chemical Research, Vol. 35, Issue 8 https://doi.org/10.1021/ar0001970	journal	August 2002
Taxonomic and Chemical Relationships Revealed by Nuclear Magnetic Resonance Spectra of Plant Exudates Lambert, Joseph B.; Wu, Yuyang; Santiago-Blay, Jorge A. Journal of Natural Products, Vol. 68, Issue 5 https://doi.org/10.1021/np050005f	journal	May 2005
Long term crop rotation effect on subsequent soybean yield explained by soil and root-associated microbiomes and soil health indicators Neupane, Achal; Bulbul, Izzet; Wang, Ziyi Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-88784-6	journal	April 2021
Antimicrobial agents from plants: antibacterial activity of plant volatile oils Dorman, H. J. D.; Deans, S. G. Journal of Applied Microbiology, Vol. 88, Issue 2 https://doi.org/10.1046/j.1365-2672.2000.00969.x	journal	February 2000
Use of Ranks in One-Criterion Variance Analysis Kruskal, William H.; Wallis, W. Allen Journal of the American Statistical Association, Vol. 47, Issue 260 https://doi.org/10.1080/01621459.1952.10483441	journal	December 1952
Preservative qualities of recent and fossil resins: Electron micrograph studies on tissue preserved in Baltic amber Poinar, George O.; Hess, Roberta Journal of Baltic Studies, Vol. 16, Issue 3 https://doi.org/10.1080/01629778500000141	journal	September 1985
Fossil fish stomachs: A microenvironment for exceptional preservation Wilby, Philip R.; Martill, David M. Historical Biology, Vol. 6, Issue 1 https://doi.org/10.1080/10292389209380416	journal	January 1992
Chemical Composition, Antimicrobial and Antioxidative Activity of Laurel, Sage, Rosemary, Oregano and Coriander Essential Oils Baratta, M. Tiziana; Dorman, H. J. Damien; Deans, Stanley G. Journal of Essential Oil Research, Vol. 10, Issue 6 https://doi.org/10.1080/10412905.1998.9700989	journal	November 1998
Comparing amber fossil assemblages across the Cenozoic Penney, David; Langan, A. Mark Biology Letters, Vol. 2, Issue 2 https://doi.org/10.1098/rsbl.2006.0442	journal	December 2005
Chemical preservation of plants and insects in natural resins Stankiewicz, B. A.; Poinar, H. N.; Briggs, D. E. G. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 265, Issue 1397 https://doi.org/10.1098/rspb.1998.0342	journal	April 1998
Contingent interactions among biofilm-forming bacteria determine preservation or decay in the first steps toward fossilization of marine embryos: Three-dimensional shape-preserving biofilms Raff, Elizabeth C.; Andrews, Mary E.; Turner, F. Rudolf Evolution & Development, Vol. 15, Issue 4 https://doi.org/10.1111/ede.12028	journal	May 2013
Nuclear Magnetic Resonance Characterization of Cretaceous Amber Lambert, J. B.; Johnson, S. C.; Poinar, G. O. Archaeometry, Vol. 38, Issue 2 https://doi.org/10.1111/j.1475-4754.1996.tb00780.x	journal	August 1996
DISTINGUISHING AMBER AND COPAL CLASSES BY PROTON MAGNETIC RESONANCE SPECTROSCOPY: Distinguishing amber and copal classes by magnetic resonance spectroscopy Lambert, J. B.; Tsai, C. Y. -H.; Shah, M. C. Archaeometry, Vol. 54, Issue 2 https://doi.org/10.1111/j.1475-4754.2011.00625.x	journal	July 2011
Nmr Analysis of Amber in the Zubair Formation, Khafji Oilfield (Saudi Arabia - Kuwait): coal as an oil Source Rock? Poinar, George; Lambert, Joseph B.; Wu, Yuyang Journal of Petroleum Geology, Vol. 27, Issue 2 https://doi.org/10.1111/j.1747-5457.2004.tb00054.x	journal	April 2004
The role of experiments in investigating the taphonomy of exceptional preservation Briggs, Derek E. G.; McMahon, Sean Palaeontology, Vol. 59, Issue 1 https://doi.org/10.1111/pala.12219	journal	November 2015
Wolbachia and Virus Protection in Insects Hedges, L. M.; Brownlie, J. C.; O'Neill, S. L. Science, Vol. 322, Issue 5902 https://doi.org/10.1126/science.1162418	journal	October 2008
Ultrastructure of 40-Million-Year-Old Insect Tissue Poinar, G. O.; Hess, R. Science, Vol. 215, Issue 4537 https://doi.org/10.1126/science.215.4537.1241	journal	March 1982
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities Lozupone, C.; Knight, R. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8228-8235.2005	journal	December 2005
A mathematical theory of communication Shannon, C. E. ACM SIGMOBILE Mobile Computing and Communications Review, Vol. 5, Issue 1 https://doi.org/10.1145/584091.584093	journal	January 2001
T HE R OLE OF D ECAY AND M INERALIZATION IN THE P RESERVATION OF S OFT -B ODIED F OSSILS Briggs, Derek E. G. Annual Review of Earth and Planetary Sciences, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.earth.31.100901.144746	journal	May 2003
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
The First Ant-Termite Syninclusion in Amber with CT-Scan Analysis of Taphonomy Coty, David; Aria, Cédric; Garrouste, Romain PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104410	journal	August 2014
Entrapment Bias of Arthropods in Miocene Amber Revealed by Trapping Experiments in a Tropical Forest in Chiapas, Mexico Solórzano Kraemer, Mónica M.; Kraemer, Atahualpa S.; Stebner, Frauke PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0118820	journal	March 2015
Paleoecology of Dominican amber preservation: spider (Araneae) inclusions demonstrate a bias for active, trunk-dwelling faunas Penney, David Paleobiology, Vol. 28, Issue 3 https://doi.org/10.1666/0094-8373(2002)028<0389:PODAPS>2.0.CO;2	journal	September 2002
Use of Ranks in One-Criterion Variance Analysis Kruskal, William H.; Wallis, W. Allen Journal of the American Statistical Association, Vol. 47, Issue 260 https://doi.org/10.2307/2280779	journal	December 1952
Exceptional Preservation of Dipteran Flight Muscle and the Taphonomy of Insects in Amber Henwood, Alison PALAIOS, Vol. 7, Issue 2 https://doi.org/10.2307/3514931	journal	April 1992

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