Earth-Science Reviews 243 (2023) 104486 Contents lists available at ScienceDirect Earth-Science Reviews journal homepage: www.elsevier.com/locate/earscirev Amber and the Cretaceous Resinous Interval Xavier Delclòs a, b, *, 1, Enrique Peñalver c, **, 1, Eduardo Barrón c, David Peris d, David A. Grimaldi e, Michael Holz f, Conrad C. Labandeira g, h, i, Erin E. Saupe j, Christopher R. Scotese k, Mónica M. Solórzano-Kraemer l, Sergio Álvarez-Parra a, b, Antonio Arillo m, Dany Azar n, o, Edwin A. Cadena p, Jacopo Dal Corso q, Jiří Kvaček r, Antonio Monleón-Getino s, André Nel t, Daniel Peyrot u, Carlos A. Bueno-Cebollada c, Alejandro Gallardo a, Beatriz González-Fernández v, Marta Goula b, w, Carlos Jaramillo x, Iwona Kania-Kłosok y, Rafael López-Del Valle z, Rafael P. Lozano c, Nieves Meléndez aa, César Menor-Salván ab, Constanza Peña-Kairath a, b, Vincent Perrichot ac, Ana Rodrigo c, Alba Sánchez-García c, Maxime Santer a, b, Víctor Sarto i Monteys ad, Dieter Uhl l, José Luis Viejo ae, Ricardo Pérez-de la Fuente af a Departament de Dinàmica de la Terra i de l’Oceà, Facultat de Ciències de la Terra, Universitat de Barcelona, Spain b Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Spain c CN Instituto Geológico y Minero de España (IGME)-Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain d Institut Botànic de Barcelona, CSIC-Ajuntament de Barcelona, Barcelona, Spain e Division of Invertebrate Zoology, American Museum of Natural History, New York, USA f Instituto de Geociências, Universidade Federal da Bahia, Salvador da Bahia, Brazil g National Museum of Natural History, Smithsonian Institution, Washington, D.C, USA h Department of Entomology, University of Maryland, MD, USA i College of Life Sciences & Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China j Department of Earth Sciences, University of Oxford, Oxford, UK k Department of Earth & Planetary Sciences, Northwestern University, Evanston, IL, USA l Senckenberg Forschungsinstitut und Naturmuseum, Frankfurt, Frankfurt am Main, Germany m Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología, Universidad Complutense, Madrid, Spain n Natural Sciences Department, Faculty of Science II, Lebanese University, Fanar-El-Matn, Lebanon o State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China p Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, Colombia q State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, China r National Museum, Prague, Czech Republic s Department de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Spain t Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, CP50 Paris, France u School of Earth Sciences, University of Western Australia, Crawley, Australia v Departamento de Explotación y Prospección de Minas, Universidad de Oviedo, Oviedo, Spain w Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biología, Universitat de Barcelona, Spain x Smithsonian Tropical Research Institute, Panama y Department of Biology, Institute of Biology and Biotechnology, University of Rzeszów, Poland z Museo de Ciencias Naturales de Álava, Vitoria-Gasteiz, and Cueva El Soplao, Celis, Santander, Cantabria, Spain aa Departamento de Geodinámica, Estratigrafía y Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, Spain ab Departamento de Biología de Sistemas, Universidad de Alcalá, Alcalá de Henares, Spain ac Géosciences Rennes - UMR 6118, University of Rennes, CNRS, Rennes, France ad Institut de Ciència i Tecnologia Ambientals (ICTA), Universitat Autònoma de Barcelona, Spain ae Departamento de Biología, Facultad de Ciencias, Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain af Oxford University Museum of Natural History, Oxford, UK * Corresponding author at: Departament de Dinàmica de la Terra i de l’Oceà, Facultat de Ciències de la Terra, Universitat de Barcelona, Spain. ** Corresponding author. E-mail addresses: xdelclos@ub.edu (X. Delclòs), e.penalver@igme.es (E. Peñalver). 1 (X. Delclòs), (E. Peñalver). These contributed equally to this work. https://doi.org/10.1016/j.earscirev.2023.104486 Available online 25 June 2023 0012-8252/© 2023 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 A R T I C L E I N F O A B S T R A C T Keywords: Amber is fossilized resin that preserves biological remains in exceptional detail, study of which has revolu­ Cretaceous tionized understanding of past terrestrial organisms and habitats from the Early Cretaceous to the present day. Amber Cretaceous amber outcrops are more abundant in the Northern Hemisphere and during an interval of about 54 Resin million years, from the Barremian to the Campanian. The extensive resin production that generated this Mass resin production Conifers remarkable amber record may be attributed to the biology of coniferous resin producers, the growth of resin­ iferous forests in proximity to transitional sedimentary environments, and the dynamics of climate during the Cretaceous. Here we discuss the set of interrelated abiotic and biotic factors potentially involved in resin pro­ duction during that time. We name this period of mass resin production by conifers during the late Mesozoic, fundamental as an archive of terrestrial life, the ‘Cretaceous Resinous Interval’ (CREI). 1. Introduction accumulations of continental organic matter, such as deltas, estuaries, swamps or oxbow lakes, are the most favorable sedimentary environ­ Resins are secondary metabolites synthesized by specialized cells of ments for resin fossilization (Grimaldi et al., 2000b; Martínez-Delclòs “gymnosperm” and angiosperm plants, whose composition consists of et al., 2004; Iturralde-Vinent and MacPhee, 2019). Resiniferous trees are amorphous mixtures of carboxylic acids, essential oils and isoprene- often located on emergent topography within these transitional envi­ based hydrocarbons (Langenheim, 2003). Resin production is condi­ ronments (Álvarez-Parra et al., 2021) or close to areas where resin pri­ tioned by temperature, solar radiation, evapotranspiration, and soil marily accumulated by low-energy transport, indicated by the water deficit (Allen et al., 2010; Rodríguez-García et al., 2015). The preservation of fragile resin structures (Grimaldi et al., 2000b; Perrichot, primary functions of resins relate to defense against herbivores and 2005; Rust et al., 2010; Veltz et al., 2013). The association of amber- pathogens, and as a healing mechanism, sealing wounds and vulnerable bearing deposits with coal (lignite) or other rocks rich in organic mat­ parts after damage caused by physical or biological agents (Langenheim, ter suggests episodes of inland environments flooded by marine trans­ 2003; Seyfullah et al., 2018). gression (Najarro et al., 2009; Rodríguez-López et al., 2020). Resins can remain sticky from just hours to several months after Although resin is exuded by different tissues and organs of plants, being secreted, which can ensnare organisms or parts of them —known amber deposits —at least those from the Cretaceous and whose as bioinclusions— found mostly in the same ecosystem as the resin- taphonomy has been addressed— were formed primarily by resin pro­ producing plant (Solórzano Kraemer et al., 2018). The crosslinking of duced by root tissues that generally lack bioinclusions (root resin) and, resin takes place over millions of years, resulting in gradual hardening, more minorly, by the trunk, branches, or above-soil plant parts (aerial decrease in thermal denaturation, and loss of free methyl groups, all of resin) (Langenheim, 1995; Álvarez-Parra et al., 2021), the latter of which lead to a relatively inert, hardened form called amber (Langen­ which has the potential to contain abundant bioinclusions. Although the heim, 1990; Anderson et al., 1992; McCoy et al., 2017; Solórzano- oldest fossil resin dates from the late Carboniferous (Bray and Anderson, Kraemer et al., 2020). Only a few types of resins can fossilize based on 2009), oldest amber with bioinclusions dates from the Late Triassic, their chemical composition (Anderson and Crelling, 1995; Langenheim, which preserves a few minute arthropods (Schmidt et al., 2012; 2003). Sidorchuk et al., 2015). Jurassic amber is scarce and may be associated Most amber deposits have yielded few or no bioinclusions. The with the tropical-equatorial zone, since it has been found primarily in reasons for this scarcity of bioinclusions are variable, but usually relate Thailand, Italy, and Lebanon; no macroscopic bioinclusions have been to the paucity of resin production during some periods of time (this hitherto reported from this amber (Nohra et al., 2013; Neri et al., 2016). paper), where the resin was produced (under aerial or underground The oldest amber deposits rich in bioinclusions are Barremian in age conditions; Álvarez-Parra et al., 2021), and/or how long the resin (Early Cretaceous) (Maksoud et al., 2017). retained its stickiness (Solórzano Kraemer et al., 2018). Amber-bearing The Cretaceous (~145.0–66.0 Ma) represents a time of rapid outcrops that preserve bioinclusions are a type of Konservat-Lagerstätte. evolutionary turnover and diversification of organisms. From a macro­ Indeed, the preservation of organisms in amber is exceptional and differs ecological perspective, it was a key period in Earth history in which the from other organic or inorganic mechanisms that retain organismic Angiosperm Terrestrial Revolution (ca. 100 to 50 Ma), inclusive of the detail for millions of years (Martínez-Delclòs et al., 2004; Ross, 2009; formerly defined Cretaceous Terrestrial Revolution (Lloyd et al., 2008; Grimaldi and Ross, 2017). Despite taphonomic biases inherent in resin Benton et al., 2022), occurred. During this time, the Mesophytic pale­ entrapment (Solórzano Kraemer et al., 2018), amber can provide obiome dominated by “gymnosperms” was replaced by a Cenophytic exceptional external and internal anatomical detail of the bioinclusions paleobiome dominated by angiosperms (Labandeira, 2014b; McElwain, and evidence of past animal behaviors (Labandeira, 2014a; Grimaldi, 2018; Birks, 2020; Condamine et al., 2020). This turnover altered the 2019). Amber deposits are typically parautochthonous-allochthonous, base of trophic networks within continental ecosystems (Labandeira, in which resin was dislodged by gravity, transported and concentrated 2014b), substantially modifying communities of herbivores (Lab­ by water, and accumulated in a primary or secondary location (Martí­ andeira, 2007; Kergoat et al., 2014) and, therefore, affecting the nez-Delclòs et al., 2004). However, a few autochthonous- composition and evolution of continental biotas (Meredith et al., 2011; parautochthonous deposits are known, in which resin experienced McKenna et al., 2015; Peris et al., 2017; Benson et al., 2021; Peris and minimal to virtually no transport (Schmidt et al., 2012; Seyfullah et al., Condamine, 2023). 2018; Álvarez-Parra et al., 2021). The climate of the Cretaceous was warmer and more humid than that Resin crosslinking, which begins once the resin is exuded by the of today, probably due to very active, sustained volcanism associated plant, continues after burial in sealed, anoxic sediments (e.g., within or with unusually extensive seafloor spreading that elevated atmospheric under layers of clay) that have little interaction with meteoric water CO2 and O2 values (Royer et al., 2004; Poulsen and Zhou, 2013). During (Martínez-Delclòs et al., 2004). Resin has almost the same density as most of the Cretaceous, polar regions were virtually devoid of ice freshwater but is buoyant in sea water or in freshwater with sediments in (Scotese, 2021) and continental land masses were largely occupied by suspension and is therefore easily transported by flotation and concen­ forests dominated by conifers (Hay and Floegel, 2012; Peralta-Medina trated by currents. For these reasons, transitional settings with large and Falcon-Lang, 2012), thereby significantly reducing albedo. The 2 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 decrease in latitudinal desert belts during the Early Cretaceous and long- However, the identity of Cretaceous resin-producing plants remains lasting humid conditions during the Late Cretaceous were driven by the unknown in most cases. The taxonomic affinities of Cretaceous trees that breakup of Pangea (Chaboureau et al., 2014; Landwehrs et al., 2021). produced abundant resin remain elusive for a variety of reasons, which Cretaceous amber-bearing deposits, at least those currently docu­ include extensive chemical variation observed in the composition of mented, have a limited temporal and geographical distribution (Martí­ Cretaceous amber samples (Menor-Salván et al., 2016; McCoy et al., nez-Delclòs et al., 2004; Labandeira, 2014a). They are known from the 2021), molecular convergence (Bray and Anderson, 2009), and the Valanginian to the Maastrichtian, but they are particularly abundant usually scarce record of plant remains in amber as bioinclusions (Kvaček and significant from the Barremian to the Campanian (these ages et al., 2018; Moreau et al., 2020). Nevertheless, geochemical studies ranging from 125.77 to ~72.1 Ma at present), and, although numerous have ruled out angiosperms as resin-producing plants during the and widely distributed, occur predominately in the Northern Hemi­ Cretaceous (Anderson et al., 1992; Lambert et al., 1996; Menor-Salván sphere, which may reflect present-day sampling biases (Fig. 1A). Several et al., 2016), with a few minor exceptions (Grimaldi et al., 2000a). Most Cretaceous amber-bearing deposits yield abundant amber and bio­ likely, angiosperms did not acquire the ability to produce resin in suf­ inclusions (Martínez-Delclòs et al., 2004; Penney, 2010; Seyfullah et al., ficient quantities to form amber-bearing deposits until the Early Eocene 2018). The most studied fossiliferous amber-bearing outcrops from the (Jossang et al., 2008). As for “gymnosperms”, the coniferous tree fam­ Cretaceous are found in Lebanon (Barremian), Congo (Aptian), Spain ilies of Araucariaceae, Cheirolepidiaceae†, Cupressaceae s.l., Podo­ (Albian), France (Cenomanian), Myanmar (Cenomanian), New Jersey in carpaceae, and Pinaceae were widely distributed during the Cretaceous the USA (Turonian), Taimyr in Russia (Santonian) and western Canada (Peralta-Medina and Falcon-Lang, 2012) (Fig. 2) and have been identi­ (Campanian). In addition to these localities, amber (with or without fied as likely resin sources of Cretaceous amber deposits (Azar et al., bioinclusions) has been reported from Cretaceous deposits in many 2010; Peñalver and Delclòs, 2010; Perrichot et al., 2010; Nohra et al., other regions worldwide (Fig. 2; Supplementary data A). 2014; Menor-Salván et al., 2016; McCoy et al., 2021) (Supplementary Molecularly analyzed amber, Pleistocene and Holocene copals, and data B). The Erdtmanithecales†, a group of non-coniferous “gymno­ Defaunation resin (produced after the beginning of the Industrial Rev­ sperms” related to the Gnetales or the Bennettitales†, and namely known olution, see Solórzano-Kraemer et al., 2020) are valuable tools for for their pollen, have been suggested as possible producers of resin that interpreting the botanical origin of amber (McCoy et al., 2017, 2021). generated amber deposits in the Aptian of Brazil (Seyfullah et al., 2020). Fig. 1. Paleolatitudinal distribution of 239 Cretaceous amber-bearing deposits, grouped by geological age (A) and sea level changes (B) throughout the Cretaceous. Amber-bearing deposit data are provided in Supplementary data A. Amber deposits represented by thin blue stripes of the same thickness; deposits within the same age box and close in paleolatitude appear as stripes of greater thickness due to superposition. Proportion of area occupied by land indicated in shades of brown (modified from Landwehrs et al., 2021: Fig. 3). Representative amber deposits: 1- Hastings (UK); 2- Golling (Austria); 3- Isle of Wight (UK); 4- Twenty-nine localities in Lebanon, Zarzar Lake (Syria); 5- Chōshi (Japan); 6- Doumanga (Congo); 7- Araripe (Brazil); 8- Ariño (Spain), Hkamti (Myanmar), Estoril (Portugal), Archidona (Ecuador); 9- Eleven localities in Spain, Salignac-Eyvigues (France), Wadi Zerqa (Jordan); 10- Six localities in France, Kachin (Myanmar); 11- Nizhnyaya Agapa (Russia), Agdzhakend (Azerbaijan); 12- Chatham Island (New Zealand); 13- Sayreville in New Jersey (USA), La Garnache (France); 14- Shavarshavan (Armenia); 15- Five localities in Taymyr (Russia), Kuji (Japan), Piolenc (France); 16-Ajka (Hungary), Eutaw Fm. in Alabama (USA), Tuna-1 (Australia); 17- Cedar Lake, Grassy Lake (and other localities, Canada); 18- Tilin amber (Myanmar); 19- Arctic Coastal Plain in Alaska (USA); 20- Hanna Basin in Wyoming (USA); 21- Hell Creek Fm. in South Dakota (USA). Eustatic sea-level changes modified from Ray et al. (2019) and after Haq (2014). Geological Timetable based in the International Commission on Stratigraphy (v 2023/06), https://stratigraphy.org/chart. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) 3 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 Fig. 2. Distribution of resiniferous forests based on known amber-bearing localities and known occurrences of potential coniferous resin-producing tree families throughout the Cretaceous: Araucariaceae, Cheirolepidiaceae†, Cupressaceae, Pinaceae, and Podocarpaceae. The dataset/sources related to the paleobotanical groups used to construct this figure is formed by Supplementary data B (data from Peralta-Medina and Falcon-Lang (2012) and our own bibliographic search) and data downloaded from Paleobiology Database (https://paleobiodb.org). A) Berriasian–Hauterivian; B) Barremian–Albian; C) Cenomanian–Turonian; D) Con­ iacian–Maastrichtian. Paleogeographic maps obtained from Scotese et al. (2021). The present-day spatial coordinates and ages from a total of 299 Cretaceous amber outcrops and 1252 paleobotanical records were obtained from a bibliographic survey (Supplementary data A and B, respectively). Present coordinates of amber outcrops and paleobotanic occurrences were rotated to paleocoordinates using R v.4.0.4 and GPlates v.2.2.0. Map visualization and imaging was made using QGIS v.3.22.3 software. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) Actuotaphonomic studies (Peñalver et al., 2018), plant bioinclusions (Fig. 5B). Photographs and data used in the figures are our own when not (Kvaček et al., 2018; Moreau et al., 2020) (Fig. 3A− B), and examination specified in the captions. of wood logs and cone scales with embedded amber in amber-rich levels (Perrichot, 2005; Mays et al., 2019) provide important evidence for 2. Definition of the Cretaceous Resinous Interval determining specific conifer taxa involved in resin mass production during the Cretaceous. Although modern Pinaceae resin is poorly We define the Cretaceous Resinous Interval (CREI) as global mass crosslinked due to its molecular composition, a few moderate-size amber resin production and burial interval that occurred from the Barremian to the deposits resulting from this resin have been found (Bray and Anderson, Campanian stages of the Cretaceous Period. We posit that, during a rela­ 2008; Menor-Salván et al., 2016). Cretaceous Cupressaceae produced tively continuous time interval of about 54 million years, a suite of resin but generally in small amounts (e.g. Otto et al., 2000). factors led to the formation of rich amber deposits with similar char­ Cheirolepidiaceae† conifers lack resiniferous structures, except for some acteristics and of wide geographic distribution (Figs. 1, 2). This time- taxa presenting traumatic resin canals (Bodnar et al., 2013; Rombola delimited interval is based on the known geological record, which pro­ et al., 2022). vides evidence of numerous amber-bearing deposits (Supplementary In this contribution, we define and outline the Cretaceous Resinous data A) from the Barremian (Early Cretaceous), namely those from Interval (CREI) by integrating diverse lines of evidence and analyzing Lebanon (Maksoud et al., 2022), to the Campanian (Late Cretaceous), the set of interrelated abiotic and biotic factors that characterized this particularly Canadian (McKellar et al., 2008) and Tilin in Myanmar interval. The data presented herein was compiled from the literature and (Zheng et al., 2018) ambers. Most of these amber deposits occur in the our own fieldwork in Cretaceous amber localities from Lebanon, Jordan, Northern Hemisphere, between 5o and 75o N paleolatitude, and are Congo, Ecuador, Spain, France, Myanmar, USA, and New Zealand; especially abundant in low to mid latitudes from the Barremian to Cenozoic amber localities from France, Mexico, Dominican Republic, Coniacian and in mid to high latitudes from the Santonian to the Cam­ New Zealand, India, China, and Ethiopia; and copal and Defaunation panian (Fig. 1A). Some Cretaceous amber-bearing deposits are found in resin deposits from Colombia, Dominican Republic, New Caledonia, the Southern Hemisphere between the Aptian–Turonian, but they are New Zealand, and Madagascar. In the latter three regions, our fieldwork scarce (Fig. 1A). Cenozoic amber deposits first appear during the Mid focused on actuotaphonomic processes aimed at understanding the Paleocene of Wyoming, USA (~61 Ma) and Late Paleocene of Alaska, conditions of production and conservation of Defaunation resin and the USA (~57 Ma) (Grimaldi et al., 2000a, 2018), and the Eocene of Oise, formation of copal deposits. France (~53 Ma), Fushun, China (53–50 Ma) and Cambay, India The materials figured in this work are housed at the El Soplao Cave (~52–50 Ma) (Jossang et al., 2008; Rust et al., 2010; Wang et al., amber collection, Spain (Figs. 3A, E, 5C), the University of Barcelona, 2014a). Spain (Figs. 3B, 5D), the Nanjing Institute of Geology and Palaeontology, There are five primary shared characteristics among amber deposits China (Fig. 5A), and the Museu de Ciències Naturals de Barcelona, Spain formed during the CREI. First, resin production was restricted to conifers 4 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 Fig. 3. Mass resin tree producers and development of fires during the Cretaceous. A) Aerial amber piece with surface imprints and bioinclusions of Frenelopsis (Cheirolepidiaceae†) axes, from the Albian of El Soplao (Spain); based on taphonomic studies, the largest number of plant bioinclusions corresponds to this resin- producing tree (Peñalver et al., 2018); B) One of the most abundant plant remains in the Cenomanian amber of Kachin (Myanmar) are axes with leaves of arau­ cariaceans (Poinar et al., 2007) (University of Barcelona); C) Charcoal from the Albian amber-bearing outcrop of San Just, level SJ2 (Spain), commonly found in amber-bearing levels (Peñalver and Delclòs, 2010); D) Agathis ovata from Col de Yaté, New Caledonia, producing copious quantities of resin in an area burned several years ago; E) The immature insect related to green lacewings, Hallucinochrysa diogenesi (Neuroptera: Chrysopoidea), from the Albian amber of El Soplao (Spain), preserved with a debris-carrying packet of trichomes with gleicheniaceous affinity; today, gleicheniacean ferns opportunistically colonize burned areas (Pérez-de la Fuente et al., 2012); F) Orthosyntexys elegans, a wasp from the relict family Anaxyelidae (Hymenoptera: Symphyta) from the Cenomanian amber of Kachin, Myanmar; the living representatives of this family lay eggs in the sapwood of conifers, preferring recently burned wood (Gao et al., 2021), photograph courtesy of T. Gao; G) Eophylica priscastellata, an angiosperm flower of the family Rhamnaceae from the Cenomanian amber of Kachin (Myanmar) showing morphological specializations identical to those of modern relatives adapted to recurrent wildfires (Shi et al., 2022); photograph courtesy of C. Shi and R. Spicer. Abbreviations: m = mandibulo- maxillary stylets (feeding structures), t = trichomes. Scale bars = 2 mm (B, F), 1 mm (E, G), 0.5 mm (A). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) 5 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 (Araucariaceae, Cheirolepidiaceae†, Cupressaceae s.l., Podocarpaceae, particularly in the Northern Hemisphere (Brown et al., 2012; Tappert and Pinaceae) (Langenheim, 2003; Menor-Salván et al., 2010; Seyfullah et al., 2013; Supplementary data C) (Fig. 3C). Third, when bioinclusions et al., 2018). Second, charcoal, resulting from plant material charred by are preserved, they correspond to similar fauna and flora under com­ wildfires, is commonly found in the same stratigraphic level as amber, parable biases (Penney, 2010; Solórzano Kraemer et al., 2018), although Fig. 4. Oxygen (O2) and carbon dioxide (CO2) atmospheric composition, temperature, and Large Igneous Province (LIP) activity throughout the Cretaceous. A) Reconstruction for Cretaceous atmospheric O2 mixing ratio (from Mills et al., 2016). Forward models of O2 based on nutrient/weathering (1, 5, 7), including isotope mass balance models (4, 8) and “proxy inversion” methods that estimate atmospheric oxygen by reference to geochemical data, assuming relationships between O2 concentration and either fossil charcoal abundance (3), carbon-to‑phosphorus ratios in sediments (6), carbon isotope composition of plant resins (9), or combined estimates for sedimentation rate and abundance of organic carbon and pyrite in rock samples (2). Also represented: wildfire minimum (for ignition) and maximum (in the Phanerozoic, Carboniferous–Permian). References used: 1- Bergman et al. (2004), 2- Berner and Canfield (1989), 3- Glasspool and Scott (2010), 4- Berner (2009), 5- Arvidson et al. (2013), 6- Algeo and Ingall (2007), 7- Hansen and Wallman (2003), 8- Falkowski et al. (2005), 9- Tappert et al. (2013); B) Comparison of the carbon isotope composition of leaves of the Cheirolepidiaceae† conifer Frenelopsis (δ13Cleaf, in green) with the evolution of the carbon isotope composition of atmospheric CO2 (δ13CCO2, in brown), from Barral et al. (2017). The Frenelopsis samples from the upper Barremian–lower Santonian interval come from amber outcrops; C) Reconstructed Cretaceous Sea Surface Temperature (SST) (from Martin et al., 2014 in Barral et al., 2017), Global Average Temperature (GAT) (from Scotese et al., 2021) and LIP running average every 5 Ma (from Eldholm and Coffin, 2000). Geological Timetable based in the International Commission on Stratigraphy (v 2023/ 06), https://stratigraphy.org/chart. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) 6 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 often bioinclusions are absent likely due to taphonomic reasons. Fourth, Cretaceous (Holz, 2015; Landwehrs et al., 2021) (Fig. 4C), with gener­ resin accumulation occurred in transitional sedimentary environments ally elevated temperatures and reduced latitudinal temperature gradi­ under subtropical and temperate paleoclimates. And fifth, resin accu­ ents between the equator and the poles of ≤35 ◦ C mean annual mulation coincides with the maximum regressive surface (or trans­ temperature (MAT) in both hemispheres (O’Brien et al., 2017; Huber gressive surface) (Bowen and Jux, 1987; Villagómez et al., 1996; Najarro et al., 2018) compared with current values. The Northern Hemisphere et al., 2009) (Fig. 1B). Spatially, the CREI appears to be global in nature, thermal gradient showed a ca. 5 ◦ C decrease from the Late Jurassic into since amber-bearing outcrops are distributed worldwide throughout the the Late Cretaceous due to increased CO2 and associated warming, while Cretaceous, although they are particularly concentrated in Laurasia and in the Southern Hemisphere the temperature gradient increased during the northern margin of Gondwana (Figs. 1, 2). In any case, we use the this time due to the migration of Antarctica towards the South Pole term ‘global’ in its broader sense as we posit that the CREI did not (Landwehrs et al., 2021). Higher temperatures also brought more necessarily take place in both hemispheres simultaneously throughout extreme atmospheric precipitation regimes and the establishment of the entire interval. more extensive regions under arid or monsoonal climates (Hasegawa et al., 2012), although the latter would have been influenced more by 3. Conditional factors on resin production and preservation palaeogeography than by atmospheric gas concentration (Farnsworth et al., 2019). Two basic conditions need to co-occur in time and space to generate Continental precipitation during the mid-Cretaceous was roughly an accumulation of resin with the potential to become an amber-bearing mirrored between the Northern and Southern Hemispheres according to deposit. First, there needs to exist resin-producing plants with the ca­ coupled ocean-atmosphere general circulation simulations, with pacity to secrete large amounts of resin. Second, there needs to be a maximum precipitation at the equator that decreased steeply to a min­ suitable sedimentary setting, namely a transitional environment that imum around 30o paleolatitude, which then increased again to a peak at buries resin under anoxic conditions. Known Cretaceous amber-bearing around 50o paleolatitude (Zhou et al., 2012). This pattern situates the deposits are restricted geographically despite the worldwide distribu­ bulk of Cretaceous amber deposits with bioinclusions (particularly tion of resin-producing conifers during various Cretaceous stages during the mid-Cretaceous) (Fig. 1A) in areas of moderate to relatively (Fig. 2). Consequently, potential lack of suitable depositional environ­ low average rainfall. Remarkably, the occurrence of the first significant ments for the accumulation and preservation of resin may have limited Triassic amber deposits with inclusions in northern Italy coincides with the distribution of amber-bearing deposits. However, transitional sedi­ the Carnian Pluvial Episode, associated with an important evolutionary mentary environments during major marine transgressions were equally radiation of “gymnosperms” (Roghi et al., 2022). probable anywhere on Earth’s surface, and have occurred cyclically The increase in atmospheric CO2 below the RuBisCo (the enzyme throughout time (Haq, 2014). Thus, the two conditions noted above may ribulose-1,5-bisphosphate carboxylase/oxygenase, involved in the first not fully explain the observed distribution of Cretaceous amber-bearing major step of carbon fixation) saturation limit accelerates plant photo­ deposits, such that other abiotic or biotic factors, and the confluence of synthesis and growth under present conditions (Dalling et al., 2016; several factors, likely promoted the production of resin by trees and/or Olivoto et al., 2017). In principle, such acceleration would suggest that its subsequent accumulation and preservation. These factors could be increasing atmospheric CO2 could result in higher metabolic rates and global or more localized in spatial scale and are not necessarily mutually thus increased production of secondary metabolites, such as resin (Trapp exclusive. and Croteau, 2001; Novick et al., 2012). However, related plant species may show opposite responses to CO2 changes due to differences in 3.1. Abiotic factors physiological plasticity (Berini et al., 2018; Kurepin et al., 2018), thereby limiting the ability to infer resin production by fossil plant Multiple abiotic factors were potentially related to the mass pro­ species based on CO2 concentration alone. Even so, CO2 and O2 values duction and/or accumulation of resin during the CREI. Although these might be indirectly linked with resin production, as elevated levels factors are interrelated and feedback on each other, we group them here would be expected to impact the physiological features of plants that, in to facilitate discussion: (1) atmospheric gas composition, temperature, turn, could increase the herbivorous, wood-boring or pathogenic activ­ and wildfires; (2) volcanism and changes in sea level; and (3) oceanic ity of other organisms such as arthropods or fungi (Lake and Wade, physicochemical properties and hurricanes. An overview of the global 2009; Labandeira, 2013; Couture et al., 2015; see section 3.2 below). climate throughout the CREI is provided at the end of this section. Numerous proxies suggest that atmospheric O2 increased continu­ ously from the Barremian to the late Cenomanian (Fig. 4A) to about 3.1.1. Atmospheric gas composition, temperature, and wildfires 29%–31% (Berner, 2006; Glasspool and Scott, 2010; Brown et al., 2012), Atmospheric gas composition (Fig. 4A− B) has a major effect on but decreased from the Turonian to the end of the Paleocene to the climate. Atmospheric greenhouse gases such as carbon dioxide (CO2) current value of 21% (Wade et al., 2019). The high O2 content in the and methane (CH4), as well as oxygen (O2) may have directly or indi­ atmosphere during the Cretaceous favored recurrent wildfires in conif­ rectly impacted global resin production. Estimates of atmospheric CO2 erous forests (Belcher and McElwain, 2008), which were also promoted concentration during the Cretaceous vary according to the authors and by increased electrical storms and intensive volcanism (Scott, 2018). proxies used (Tappert et al., 2013; Landwehrs et al., 2021) but generally Charcoal is indicative of paleowildfires (Brown et al., 2012; Scott, 2018) is considered to have been more than twice that of preindustrial values, and is abundant in most Cretaceous amber-bearing deposits (Peñalver between 560 and 1680 ppm (Barral et al., 2017). and Delclòs, 2010; Shi et al., 2012; De Lima et al., 2019) (Fig. 3C), but High CO2 levels are due to extensive volcanic emissions during the mainly in the Northern Hemisphere deposits (Supplementary data C), Cretaceous from Large Igneous Provinces (LIPs, Fig. 4C) and seafloor including the presence of charcoalified remains within amber (Grimaldi formation (Condie et al., 2021). Wildfires, changes in ocean chemistry, et al., 2000b; Najarro et al., 2010). Partially burned amber pieces have biotic respiration, and organic matter decomposition also released sig­ been found occasionally together with charcoalified plant material nificant amounts of CO2 to the atmosphere during the Cretaceous (Hu (Grimaldi et al., 2000b). et al., 2012; Wang et al., 2014b; Scott, 2018). Methane has a greater Extant trees increase resin exudation if injured by fire (Fig. 3D) as a greenhouse potential than CO2, and is likely to have notably increased physiological response that prevents pathogenic activity or arthropod during the Cretaceous (Jahren et al., 2001; Chang et al., 2022). Higher invasion (Langenheim, 2003; Della Prasetya et al., 2017). Fire has CH4 levels were related to the liberation of methane hydrate from the played a key role in reshaping ecosystems, particularly after the accu­ seafloor by rising water temperatures (Wagner et al., 2007) and from mulation of flammable biomass arising from increased productivity of seafloor spreading. Global temperatures fluctuated during the terrestrial ecosystems linked to the predominance of angiosperms (Bond 7 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 and Scott, 2010) and from the altered ignitability and flammability of 3.1.3. Oceanic physicochemical properties and hurricanes angiospermous plant matter (Belcher and Hudspith, 2017). Different Amber-bearing deposits are frequently associated with transitional groups of Cretaceous conifers exhibit pyrophilous modifications linked sea-to-land environments. Thus, the properties of ocean waters, namely to recurrent wildfires (He et al., 2016), in lifestyles such as serotiny that salinity and sea surface temperature (SST), and paleocirculation pat­ has endured into the present (Pausas, 2018). Moreover, there are diverse terns may have affected the formation of resin deposit. Salinity may instances of organisms associated with fire that are preserved in Creta­ have controlled the formation of resin deposits because resin has a lower ceous ambers (Ortega-Blanco et al., 2008; Pérez-de la Fuente et al., density than seawater, rendering it buoyant and making its burial and 2012; Shi et al., 2022) (Fig. 3E− G). preservation in environments with high salinity difficult. High salinity The above lines of evidence suggest wildfires played a role in the conditions did occur in regions where amber-bearing deposits are found genesis of resin deposits during the CREI, at least in some deposits, by in the Northern Hemisphere, such as Myanmar and New Jersey of the favoring resin exudation but also subsequent accumulation, since USA (Poulsen et al., 1998; Ladant et al., 2020; Topper et al., 2011), and deforested soils experienced increased erosion. However, based on the Brazil and the Congo in the Southern Hemisphere (Pérez-Diaz and Ea­ global occurrence of wildfires (Brown et al., 2012; Scott, 2018; Sup­ gles, 2017). However, the formation of resin deposits in high salinity plementary data C) and the broad distribution of potential resiniferous zones suggest only temporary marine influence. The record of frequent, plants during the CREI (Fig. 2; Supplementary data B), a global distri­ yet rarely diverse, marine protists and invertebrates, such as oysters or bution of Cretaceous amber deposits would be expected, for which there crinoids, and plant macroremains in amber deposits (Néraudeau et al., is currently no evidence (Fig. 2). Wildfires were globally distributed but 2008; Barrón et al., 2015; Peyrot et al., 2019) supports a transitional seems only involved in local and regional resin production and accu­ depositional setting with occasional marine influence. mulation during the CREI (e.g., the Raritan Fm. amber in New Jersey, Global average SST during the mid-Cretaceous was >6 ◦ C higher USA or Spanish and French ambers), but appear not to be a definitive than that of today (Hay, 2009; Torsvik and Cocks, 2016), but disparate cause of resin production on a global scale. data exist regarding SSTs throughout the entire Cretaceous (Hay and Floegel, 2012) (Fig. 4C). Global ocean circulation changed significantly 3.1.2. Volcanism and changes in sea level during the Cretaceous due to progressive opening of the South Atlantic The abundant record of volcanic rocks associated directly or laterally Ocean and the Tethyan Circumglobal Current, providing east to west with Cretaceous amber-bearing deposits such as those in Lebanon (Veltz flow around the globe at low latitudes of the Northern Hemisphere. In et al., 2013), Myanmar (Shi et al., 2012), Ecuador (Balseca et al., 1993), addition, the transfer of heat from the hydrosphere to the atmosphere and Canada (Eberth, 2005) is evidence that resin mass production took from water vapor played an important role in cooling the tropics and in place in environments amid local volcanic influence, with this factor warming at high latitudes, establishing the diminished latitudinal intimately related to wildfires (see above). Aside from increasing at­ gradient of temperature noted earlier. These factors conditioned global mospheric O2 concentrations that promoted wildfires, large amounts of temperature and climate during the CREI (Hay, 2009; Wohlwend et al., volcanic emissions over a long period of time in LIPs could have affected 2015), and thus may have indirectly impacted resin formation and/or global climate in other ways (Johansson et al., 2018; Macdonald et al., accumulation. 2018). The maximum development of LIPs during the last 2500 million Linked to high average SST during the Cretaceous (O’Brien et al., years occurred during the Cretaceous (Eldholm and Coffin, 2000; Condie 2017), heavy rainfall and winds, such as those during hurricanes, have et al., 2021). This peak of LIP development (Fig. 4C) altered atmospheric been proposed as an abiotic cause of resin production. High winds can composition and circulation patterns and changed the geometry of cause severe damage to trees, which is sealed by resin to minimize sedimentary basins and sea level. The formation of LIPs and seafloor opportunistic insect attacks or pathogenic infections (Langenheim, spreading, in combination with increased global MATs, led to the 1994; Seyfullah et al., 2018). Climate models based on marine and melting of polar ice caps (Zhou et al., 2008; Hay, 2017) and to signifi­ continental distribution and topography suggest winds were generally cant reductions in the Earth’s albedo (Kent and Muttoni, 2022) during weaker during the Cretaceous than at present (Cousin-Rittemard et al., the Cretaceous. These changes produced a global marine transgression 2002; Hay, 2009), but the consistently high annual SST could have trend (Fig. 1C) from the Valanginian to the Turonian (Wagreich et al., promoted the development of hurricanes in low to mid latitudes. The 2020). This global transgression was only interrupted by a regression at absence of high topographic relief (Hay et al., 2019) would have allowed the Aptian− Albian boundary, after global MATs (Haq, 2014) fell to the wind to circulate without diverting its zonal flow (Scotese et al., 12 ◦ C (Hay, 2017). Maximum transgression was reached in the Turonian 2021). and sea level remained at high stands into the Campanian (Olde et al., 2015). All resin-bearing deposits were developed in periods of maximum 3.1.4. Climatic overview throughout the CREI regression, onlapped by the second-order marine transgressive strata Based on paleoclimate data and maps (Chumakov et al., 1995), most (Grimaldi et al., 2000b; Perrichot, 2005; Najarro et al., 2009) (Fig. 1C). Cretaceous amber-bearing deposits originated in the northern mid- The globally-high sea level during the CREI increased insularization, latitude warm humid belt. Nevertheless, during the Albian and Santo­ changing the extent and distribution of land masses and epicontinental nian, some amber-bearing localities were present well within the seas such as the Late Cretaceous European archipelago, and the Mid­ northern high-latitude temperate humid belt, and during the Albian and continental Seaway of North America. Extensive regions were flooded, Cenomanian other amber-bearing localities were present within the which produced the remobilization of abundant resin stored in the soils equatorial humid belt and northern hot arid belt, respectively. Based on due to erosion resulting from the transgressions, establishing new areas global circulation models, the depositional environments that gave rise of shallow deposition, reducing terrestrial biotopes, and increasing to amber-bearing deposits in Lebanon (Barremian) were located within flooding stress (Erwin, 2009). Marine transgressions have been associ­ the tropical climate belt (Sewall et al., 2007; Ohba and Ueda, 2010). ated with higher global temperature and paleogeographic changes, both During the lower to middle Aptian, the climate cooled globally (Mut­ of which caused more emergent land masses at mid to high latitudes in terlose et al., 2010), which coincides with a reduction in currently the Northern Hemisphere (Landwehrs et al., 2021), which potentially known amber deposits, although this cold interval was recently ques­ allowed for more colonization by plants and distribution of coniferous tioned (Huber and O’Brien, 2020). forest (Klages et al., 2020). This pattern contrasts with what occurred in At the Aptian–Albian boundary, warm greenhouse conditions were the Southern Hemisphere during the Cretaceous, wherein the proportion re-established due to intense volcanism, coinciding with amber deposits of emerged land masses at mid to high latitudes remained low, similar in in Brazil, Ecuador, and the Congo at low latitudes in the Southern extent to that of the present day (Figs. 1, 2). Hemisphere (Pereira et al., 2009; Cadena et al., 2018; Bouju and Per­ richot, 2020). During the Albian, an extensive subtropical arid belt 8 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 developed in the equatorial zone, which subsequently migrated pole­ herbivory during the CREI in rock deposits (Labandeira, 1998, 2014b; ward (Scotese, 2021). Abundant resin accumulations were common in Xiao et al., 2022a, 2022b), and there has been no assessment of the tropical mid latitude areas, such as Iberia, leading to the present-day herbivory in amber due to the scarcity of damaged leaves and other Spanish amber deposits (Peñalver and Delclòs, 2010). photosynthetic structures (such as cheirolepidiacean axes) as During the Cenomanian–Turonian, climate zones began to organize bioinclusions. latitudinally (Sewall et al., 2007), although still under hothouse condi­ Pathogenic organisms can invade plant tissues directly or through a tions (Kidder and Worsley, 2010; Mills et al., 2017), enabling the trop­ vector. Aside from their ability to cause direct harm, some extant species ical biota to migrate poleward of 40oN latitude. Although currently there from insect groups transmit pathogens to their plant hosts, including are important forests of conifers in very high latitudes (Fig. 2), resin viruses, bacteria, fungi, oomycetes, and nematodes (Labandeira and deposits were formed at that time mostly between 30o and 40oN lati­ Prevec, 2014). tude, with some exceptions at higher latitudes (Fig. 1), corresponding to The development of insect-borne pathogens depends on population a MAT of around 30 ◦ C (Hay and Floegel, 2012); these conditions may dynamics, dispersal ability, host selection behavior, and the feeding have produced the resin corresponding to amber-bearing deposits from behavior of the insect vectors (Labandeira and Prevec, 2014; Eigenbrode the lower Cenomanian of France (Perrichot et al., 2010), Myanmar (Ross et al., 2018). Bacteria and fungi are chiefly spread by adhering to the et al., 2010), and from the Turonian of New Jersey in the USA (Grimaldi insect’s body, so their vector relationship is not as specific as that which and Nascimbene, 2010). occurs in the transmission of viral diseases (Jones, 2005). Oomycetes are During the upper Turonian–Maastrichtian, climate changed consid­ remarkable plant pathogens, because infection by these fungus-like erably (Tabor et al., 2016). Simulated global mean surface air temper­ microorganisms can induce copious resin exudation, as observed in atures (GMST) show temperatures of 21.2 ◦ C–19.5 ◦ C during the the genus Agathis in New Zealand (Fig. 5E− G), which produces a Campanian. These cooling trends are associated with changes in the particular variation in the color of large resin exudates (Weir et al., fraction of Earth’s surface occupied by land (Fig. 1B), which has a higher 2015). Unfortunately, this type of resin would be difficult to recognize average albedo than that of the ocean, caused by lower sea levels that once transformed into amber; future studies may be able to distinguish resulted in greater exposure of continental areas (Landwehrs et al., this resin isotopically or by the presence of oomycete spores as 2021). Although average global temperatures decreased during the bioinclusions. Turonian–Maastrichtian, most resin deposits formed at high latitudes, Plants are known to emit volatile compounds to attract or repel in­ namely of the Northern Hemisphere, and were rare at mid to low lati­ sects (Raffa, 2014; Pichersky and Gershenzon, 2020). However, many tudes (Fig. 1B). From this interval are known the amber deposits of the insect species are attracted to volatile plant mixtures that indicate stress, Santonian from the Taymyr region in Russia (Perkovsky and Vasilenko, as this signaling can allow insects to enter tissues free of defense and, 2019), from the Campanian of Cedar Lake and Grassy Lake in Canada potentially, competition (Hulcr and Dunn, 2011). Angiosperm resin (McKellar et al., 2008), and from the Campanian–Maastrichtian of the terpenoids attract insect pollinators (Armbruster, 1984; Boncan et al., Arctic Coastal Plain in Alaska (Langenheim et al., 1960). 2020). Highly specialized pollination relationships between some groups of insects and “gymnosperms” have been discovered in amber 3.2. Biotic factors since the Albian (Fig. 5C), in some instances lacking extant representa­ tives of such pollination interactions (Peñalver et al., 2012, 2015; Peris The mass production of resin during the CREI may have been pro­ et al., 2017, 2020; Peña-Kairath et al., 2023). Resin exudation by co­ moted by biotic factors acting at a regional scale (Martínez-Delclòs et al., nifers during the CREI could be related to the attraction of certain groups 2004; Seyfullah et al., 2018). These factors include arthropod damage, of insects to assist in pollination. This idea was proposed for Cenozoic pathogenic activity, and the emission of volatile compounds by the ambers produced by angiosperms (Armbruster, 1993). The hypothesis is resins to attract pollinators and other insects (Langenheim, 1994; challenging to test at present, and the absence of Cretaceous insects with Pichersky and Gershenzon, 2020; Peris et al., 2021). attached coniferous pollen (Peris et al., 2020) renders it unlikely. Terrestrial arthropods (insects, mites) can cause severe damage to Nevertheless, cheirolepidiaceous pollen has been found on the mouth­ plants through feeding- or development-related activity. Different parts of insects in compression–impression deposits from non-amber wood-boring insects, namely beetles (Coleoptera), but also some wasps producing environments of the Middle Jurassic to the Early Creta­ such as wood wasps (Hymenoptera: Siricidae) and moths such as cossid ceous (Labandeira et al., 2016), indicating insect pollination of at least millers or clearwing moths (Lepidoptera: Cossidae and Sesiidae), bore one reproductively specialized cheirolepidiaceous conifer was an into wood for nest building and offspring development, at times culti­ exception (Labandeira et al., 2007). vating fungi as a food source in galleries within woody tissues (Hulcr and Stelinski, 2017; Peris et al., 2021). The diseased tree reacts against 4. Present limitations and future directions invasive agents by developing secondary defensive compounds such as terpene-rich oleoresins in conifers, which flood the area to physically We propose that the CREI represented a distinct mass resin produc­ repel the invasion, while different toxins and volatiles act as a chemical tion that occurred over a continuous time interval from the Barremian to defense (Raffa, 2014; Krokene, 2015). The influence of massive attacks the Campanian, despite differences in the known record of amber- of wood-boring beetles on resiniferous ancient forests has been widely bearing deposits between Cretaceous geochronologic stages (Fig. 1A). cited in the literature based on their abundance in Cenozoic ambers, The causal mechanisms underlying such fluctuations are not well un­ Pleistocene and Holocene copals, and Defaunation resins (Martínez- derstood, although they may relate to circumstances that are best Delclòs et al., 2004; Labandeira, 2014a; Seyfullah et al., 2018; Peris, studied on a case-by-case basis by integrating multiple approaches. 2020). However, there is no significant direct evidence of beetle in­ Although we hypothesize that the same set of general processes that festations in Cretaceous ambers yet found, although scarce wood boring promoted resin mass production and accumulation acted for the entirety beetles such as auger beetles (Bostrichidae), spider beetles (Ptinidae), of the CREI, we posit that these were under the influence of possible ship timber beetles (Lymexylidae) and weevils (Curculionidae) are local or regional controls that determined the intensity of the effect. The found occasionally (Chen and Zhang, 2020; Peris, 2020; Peris and Rust, relative importance of the abiotic and biotic factors influencing resin 2020) (Fig. 5A− B). Herbivorous insect groups such as true bugs (Hem­ production and accumulation during the CREI at regional geographical iptera), thrips (Thysanoptera) (Fig. 5D), grasshoppers and crickets scales, among other variables, will need to be rigorously tested in future (Orthoptera), and termites (Isoptera) have been found in major Creta­ studies. ceous amber deposits, including taxa that currently cause significant We established the CREI with a stage/age hierarchy (apud IUGS damage to plants. However little evidence exists of intense arthropod Chronochart - Gradstein et al., 2021). Finer temporal resolution would 9 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 Fig. 5. Biotic factors that could have promoted resin mass production during the Cretaceous: wood-boring insects, pollination, and pathogens. A) A lymexylid beetle; larvae of this group of beetles today penetrate living and decaying wood, consuming fungus in a symbiotic association; unpublished specimen from the Nanjing Institute of Geology and Palaeontology, China Academy of Sciences; B) Bostrichid beetles Cretaretes minimus, from Kachin amber (Peris and Jelínek, 2020); these beetles could have been among the first wood-boring beetles and transmitters of pathogens; C) The zhangsolvid fly Buccinatormyia magnifica, from El Soplao amber (Peñalver et al., 2015); the oldest instances of “gymnosperm” pollinators in amber are found in the Albian of Spain; D) Thrips (Thysanoptera) swarm from Kachin amber with attached pollen grains (unstudied, UB); thrips were “gymnosperm” pollinators, but this group could have also been the cause of massive attacks on resinous trees; E–G) Agathis australis (Araucariaceae) attacked by the oomycete Phytophthora agathidicida (Oomycota) in Waipoua Forest, New Zealand, causing copious resin production (E, F) and the eventual death of the tree (G). Scale bars = 1 mm (A), 0.5 mm (B), 2 mm (C), 0.2 mm (D). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) 10 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 reduce considerable noise to the analyses at present, as many amber interrelated. Abiotic conditions potentially related to massive resin deposits and conventional paleobotanical deposits are characterized by production and accumulation during the CREI include: (1) increased significant temporal uncertainty. global average temperatures, including SST, with the consequent Further work to improve temporal resolution will involve more ac­ reduction in albedo due to the absence of icy poles, (2) reduced lat­ curate dating of the deposits, more detailed identification of changes in itudinal temperature gradients, which allowed the development of for­ atmospheric gas composition, more precise evaluations of meso- and ests at high latitudes, (3) higher levels of greenhouse atmospheric gases macroplant remains from amber deposits, and other studies within each (carbon dioxide, methane) and oxygen, which promoted changes in the Cretaceous stage. These studies may provide further insight into the growth and development of the biota, (4) increased volcanic activity, causal mechanisms for enhanced resin production and accumulation which promoted an increase in temperature and changes in the during the CREI. A higher-resolution temporal framework might also composition of atmospheric gases, (5) moderate or relatively high allow identification of distinct subintervals or even events within the average rainfall that could favor the development of large forests and the Cretaceous Resinous Interval. production of resin, (6) enhanced wildfire activity due to volcanism and Although sampling bias may be an explanation for the apparently high O2 levels, (7) transgressive sea level periods and overall trend, skewed presence of amber deposits towards the Northern Hemisphere which reduced terrestrial land area but led to the filling of large areas of during CREI (Figs. 1, 2), paleogeographical circumstances may lowlands and formation of resin deposits, and (8) increased storm and contribute to explain the pattern. First, a greater proportion of land had hurricane activity that could have promoted wildfires and/or destruc­ emerged in the Northern Hemisphere (Landwehrs et al., 2021) during tion of large areas of forest, and consequently resin production. Biotic the Cretaceous, and was thus sustaining potentially greater extensions of factors partially explaining the CREI at a more localized scale could resin-producing forests. Second, different resiniferous species distrib­ include arthropod damage, pathogenic activity due to high temperatures uted among both hemispheres could have had different capacities to and humidity, and the emission of insect-attracting compounds by produce resin even under comparable environmental conditions and, resins. Future studies on the CREI will need to focus on elucidating the thus, a different potential to produce amber deposits; this has been relative importance of each of these abiotic and biotic factors, enhancing observed at present even between closely related species (Langenheim, the spatial and temporal resolution of the succession of paleoevents, 1995; Seyfullah et al., 2018). It will be necessary to substantially in­ increasing prospective efforts − particularly in the Southern Hemi­ crease reconnaissance efforts in the Southern Hemisphere to shed light sphere− , and improving taphonomic understanding of Cretaceous on this matter. amber deposits. Taphonomic knowledge on the known Cretaceous amber deposits is Our multidisciplinary approach will hopefully stimulate future scarce, fundamentally limiting understanding of the CREI. It is impera­ research efforts aimed at elucidating past dynamics between the geo­ tive to improve efforts studying amber deposits (both the amber itself sphere and the biosphere. Increased knowledge of when, how and why and the associated stratal context) from a detailed taphonomic stand­ the CREI occurred will shed light on its global impact for Cretaceous point. Such studies would aim to elucidate the paleoenvironmental, terrestrial ecology and the establishment of modern terrestrial ecosys­ paleoecological, and geological circumstances surrounding the produc­ tems. The exceptionally preserved record trapped in resin during the tion and accumulation of resin and the formation of amber. A particular Cretaceous Resinous Interval is crucial to unravel the evolutionary his­ emphasis should be on improving paleobotanical analyses of meso- and tory of many key terrestrial lineages, including plants, arthropods, and macro-remains, including fossilized wood. A focus on actuotaphonomic vertebrates, and for understanding life in a moment of critical change for experiments, both in the field and the laboratory, will further comple­ terrestrial ecosystems at the transition from the Mesozoic to the ment our view on the subject. Cenozoic. 5. Conclusions Funding The Cretaceous distribution of amber-bearing deposits is clustered This work was supported by the Spanish Ministerio de Ciencia, around an interval of roughly 54 Ma, from the Barremian to the Cam­ Innovación y Universidades [research agreement CRE CGL2017-84419 panian, and reflects global, massive resin production during the late AEI/FEDER, UE] and by the Consejería de Industria, Turismo, Innovación, Mesozoic. Prior to this interval, amber is remarkably scarce, appears in Transporte y Comercio of the Gobierno de Cantabria through the public small quantities and, save from some Triassic amber, has not hitherto enterprise EL SOPLAO S.L. [research agreement #20963 with University yielded macroscopic bioinclusions. We place the end of the interval in of Barcelona and research contract Ref. VAPC 20225428 to CN-IGME the Campanian, provided that during the Maastrichtian amber is lati­ CSIC, both 2022–2025]; the Conselho Nacional de Pesquisa (Brazil) tudinally well distributed but appears in small quantities and is scarcely [research grand PQ 304529/19–2]; National Geographic Global Explo­ fossiliferous. Shortly before the K-Pg boundary lignite deposits exist but ration Fund Northern Europa [research agreement GEFNE 127-14]; with the absence of amber that extends into the Paleocene, establishing Deutsche Forschungsgemeinschaft (DFG) [research agreement SO 894/ a gap of several million years without amber and obviously 6-1]; VolkswagenStiftung [research agreement 90946]; the Secretary of bioinclusions. Universities and Research (Government of Catalonia) and by the Hori­ In the Cenozoic the resin producers were no longer exclusively co­ zon 2020 program of research and innovation of the European Union nifers, but rather the first deposits of angiosperm resins appeared. under the Marie-Curie [research contract no. 801370, Beatriu de Pinós]; Shared characteristics of Cretaceous amber deposits are herein used to the Secretary of Universities and Research (Government of Catalonia) formally establish the Cretaceous Resinous Interval, or CREI, and are and the European Social Fund [research contract 2021FI_B2 00003]; this distinct from those shown by Cenozoic amber deposits. The resin that work is a contribution to the grant RYC2021-032907-I, funded by the generated the amber during the CREI was produced by conifers and MCIN/AEI/10.13039/501100011033 and by the European Union accumulated in transitional sedimentary environments from subtropical «NextGenerationEU»/PRTR; and the National Agency for Research and and temperate regions, commonly associated with charcoal and coin­ Development (ANID) Scholarship Program [BECAS CHILE 2020-Folio ciding with the maximum regressive surface. Moreover, the fauna and 72210321]. flora preserved within the CREI share comparable group compositional characteristics, possibly due to similar original paleoenvironment, and Author contributions suffered comparable taphonomic biases (Martínez-Delclòs et al., 2004; Solórzano Kraemer et al., 2018; Seyfullah et al., 2018). Study conception and design, contributed equally: X.D. and E.P. The potential causal factors for the CREI are complex and Data collection: X.D., E.P., D.P., D.G., M.H., C.L., Ch.S., M.M.S-K and 11 X. Delclòs et al. Earth-Science Reviews 243 (2023) 104486 R.P.-d.l.F. Belcher, C.A., Hudspith, V.A., 2017. Changes to cretaceous surface fire behaviour influenced the spread of the early angiosperms. New Phytol. 213, 1521–1532. Conducted the fieldwork and the preparation, identification, and https://doi.org/10.1111/nph.14264. analysis of the field samples: X.D., E.P., E.B., D.P., D.G., C.L., M.M.S-K., Belcher, C.M., McElwain, J.C., 2008. Limits for combustion in low O2 redefine S.Á.-P., D.A., E.C., R.L-D., A.N. and V.P. paleoatmospheric predictions for the Mesozoic. Science 321, 1197–1200. https:// Analysis and interpretation of results: X.D., E.P., D.P., D.G., M.H., C. doi.org/10.1126/science.1160978. Benson, R.B.J., Butler, R., Close, R.A., Saupe, E., Rabosky, D.L., 2021. 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