Amber! Conrad C
AMBER! CONRAD C. LABANDEIRA! Department of Paleobiology, National Museum of Natural History, Smithsonian Institution Washington, D.C. 20013 USA ˂[email protected]! ˃ and! Department of Entomology, University of Maryland, College Park, MD 20742 USA
ABSTRACT.—The amber fossil record provides a distinctive, 320-million-year-old taphonomic mode documenting gymnosperm, and later, angiosperm, resin-producing taxa. Resins and their subfossil (copal) and fossilized (amber) equivalents are categorized into five classes of terpenoid, phenols, and other compounds, attributed to extant family-level taxa. Copious resin accumulations commencing during the early Cretaceous are explained by two hypotheses: 1) abundant resin production as a byproduct of plant secondary metabolism, and 2) induced and constitutive host defenses for warding off insect pest and pathogen attack through profuse resin production. Forestry research and fossil wood-boring damage support a causal relationship between resin production and pest attack. Five stages characterize taphonomic conversion of resin to amber: 1) Resin flows initially caused by biotic or abiotic plant-host trauma, then resin flowage results from sap pressure, resin viscosity, solar radiation, and fluctuating temperature; 2) entrapment of live and dead organisms, resulting in 3) entombment of organisms; then 4) movement of resin clumps to 5) a deposition site. This fivefold diagenetic process of amberization results in resin→copal→amber transformation from internal biological and chemical processes and external geological forces. Four phases characterize the amber record: a late Paleozoic Phase 1 begins resin production by cordaites and medullosans. A pre-mid-Cretaceous Mesozoic Phase 2 provides increased but still sparse accumulations of gymnosperm amber. Phase 3 begins in the mid-early Cretaceous with prolific amber accumulation likely caused by biotic effects of an associated fauna of sawflies, beetles, and pathogens. Resiniferous angiosperms emerge sporadically during the late Cretaceous, but promote Phase 4 through their Cenozoic expansion. Throughout Phases 3 and 4, the amber record of trophic interactions involves parasites, parasitoids, and perhaps transmission of diseases, such as malaria. Other recorded interactions are herbivory, predation, pollination, phoresy, and mimicry. In addition to litter, amber also captures microhabitats of wood and bark, large sporocarps, dung, carrion, phytotelmata, and resin substrates. These microhabitats are differentially represented; the primary taphonomic bias is size, and then the sedentary vs. wandering life habits of organisms. Organismic abundance from lekking, ant-refuse heaps, and pest outbreaks additionally contribute to bias. Various techniques are used to image and analyze amber, allowing assessment of: 1) ancient proteins; 2) phylogenetic reconstruction; 3) macroevolutionary patterns; and 4) paleobiogeographic distributions. Three major benefits result from study of amber fossil material, in contrast to three different benefits of compression-impression fossils.
INTRODUCTION earliest biotas, including microbiotas and ! macroscopic inclusions. Amber first appears in Amber is a significant source of information the fossil record during the early Pennsylvanian about terrestrial forest and woodland ecosystems (~320 Ma), but lacks any significant record of from deposits of late Pennsylvanian to Pleistocene macroscopic biological inclusions until the mid- age. Although there are hundreds of sites Early Cretaceous (~125 Ma), with the sole worldwide that provide significant accumulations exception of very rare and isolated occurrence of of amber, only a small fraction of these sites have late Triassic arthropods from the Dolomites the greatest scientific potential for preserving the Region of the Southern Alps in Italy (Schmidt et In: Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. The Paleontological Society Papers, Volume 20, Marc Laflamme, James D. Schiffbauer, and Simon A. F. Darroch (eds.). The Paleontological Society Short Course, October 18, 2014. Copyright © 2014 The Paleontological Society. THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 al., 2012). Twenty-five biotically rich or contributes to amber fossil record will spark new otherwise potentially important amber deposits ways of investigating and understanding this vast have been identified (Table 1;
164 LABANDEIRA: AMBER resin or copal to recognizably fossilized amber is Pennsylvanian deposit (Bray and Anderson, a highly variable diagenetic process known as 2009). This amber type was retained in most ‘amberization.’ While inexact, copal refers to any lineages of resin-producing plants, particularly resin that is less than 40,000 years old, whereas angiosperms, and, to a much lesser extent, amber is older than 40,000 years. In addition, and gymnosperms. A different distributional pattern is without reference to geochronological age, copal found in Class II ambers, which are angiosperm in consists of resin in a deposit that retains the origin and occur in southeastern Asia and the melting point, hardness, solubility, and other southern and western areas of the United States. physiochemical properties of modern resin Class III ambers are restricted to sites in Germany (Poinar, 1992a), and is determined by the and the Atlantic Coastal Plain of the United tackiness of the resin surface. While the States. Class IV and V ambers are friable, distinction of copal versus amber remains typically are poorly preserved, and have a unsatisfactory, the definition of an ‘amber fossil’ sporadic fossil record. used by paleontologists generally refers to any Determination of the botanical source of an trace of life occurring in the amber sedimentary amber is fraught with difficulty. Various types of record regardless of its age or preservational state. identification procedures for characterizing Ambers are not true minerals because they modern resins, such as nuclear magnetic lack a crystallographic structure, although they resonance spectroscopy and pyrolysis gas are treated as such informally. Most ambers chromatography-mass spectrometry analyses may consist of complex terpenoid or phenolic reveal fossil taxa that either are closely related to, compounds linked by isoprene units or are extinct relatives of, a modern taxon. (Langenheim, 1990). Terpenoid-based ambers Alternatively, fossil resins may have been contain volatile monoterpenes, sesquiterpenes, diagenetically degraded so that molecular and some diterpenes mixed with nonvolatile comparisons to modern taxa may not be possible tripterpene and other diterpenes accompanied by (Lambert et al. 2008, 2009). Supporting alcohols, aldehydes, esters, and difficult-to- anatomical determinations should buttress characterize neutral substances (Langenheim, identifications from chemical, spectroscopic, and 1990). These compositional differences are other determinative techniques. The botanical important for segregation of ambers into sources of amber include a variety of modern chemically recognizable groups. Based on their gymnosperms and angiosperm taxa (Langenheim, macromolecular and structural properties, ambers 1995; Lambert et al., 2008), and extinct seed- are grouped into five major classes (Beck, 1999; plant taxa (Langenheim, 1990; Alonso et al., Lambert et al., 2008). Class I ambers are based on 2000; Perrichot et al., 2010; Schmidt et al., 2012). polymers or copolymers of labanoid terpenes, and Extinct late Carboniferous and Permian plant are by far the most commonly occurring type. lineages that produced modest amounts of amber Three subdivisions of Class I ambers—Subclass included medullosans (Kosanke and Harrison, 1a, 1b and 1c ambers—are each grouped based on 1957; van Bergen et al., 1995), cordaites (Jones their molecular structure, stereochemistry, and the and Murchison, 1963), and unknown seed-plant presence or absence of succinic acid and other sources (Bray and Anderson, 2009). Sources of constituents. Class II ambers are common, and Triassic to mid-early Cretaceous amber likely consist of polymers of sesquiterpenoid included the extinct Cheirolepidaceae (Roghi et hydrocarbons that are derived from cadienene. al., 2006; Schmidt et al., 2012), Araucariaceae Class III ambers are composed of polystyrene (Litwin and Ash, 1991; Philippe et al., 2005; Azar compounds. Class IV ambers are terpenoids that et al., 2010), and Cupressaceae (Grimaldi, 1996). lack the molecular structural organization of Class During the mid- to Late Cretaceous, amber I and II ambers required for polymerization, and deposits were almost entirely gymnospermous, are based on cedranes and related compounds. overwhelmingly consisting of Cheirolepidiaceae, Class V ambers similarly lack structural Araucariaceae, and Cupressaceae (Knight et al., organization for polymerization, but instead 2010; Grimaldi and Nascimbene, 2010), a pattern contain the diterpenoids abietane, pimarane, or that continued into the Paleocene, although isopimarane, and are restricted to pinaceous taxa supplemented by contributions from the Pinaceae. (Lambert et al., 2008). Angiosperm resins enter the fossil record during The earliest amber known from the fossil the mid-Late Cretaceous with the appearance of record is a Class Ic amber, occurring in an early amber attributed to Liquidambar, and
165 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 subsequently expand during the Paleogene. subtropical gymnosperms and angiosperms Paleogene occurrences include the Combretaceae (Langenheim, 1995), which also are the resins (Indian almond family), Dipterocarpaceae that readily polymerize during amberization. Such (dipterocarp family), Burseraceae (frankincense resins have the greatest fossil persistence, in part, family), and especially the Fabaceae (legume due to efficient transportation to nearby sites of family). Neogene Copaifera (copaiba), and deposition. especially Hymenaea, become prolific resin There are two hypotheses to explain why producers, responsible for the richest amber more resin is produced by certain arborescent taxa deposits from the Miocene to the Recent than others, particularly in tropical and (Langenheim, 1990; Penney and Preziosi, 2010). subtropical environments (Langenheim, 1990). Modern resin producers include all of the One hypothesis states that resin production is a previous taxa mentioned, but importantly, consist consequence of a plant’s secondary metabolism of taxa that are not found in the fossil amber resulting from the availability of carbon for record. Gymnosperms, while producing prolific synthesizing complex molecules such as amounts of resins, have a more limited number of terpenoids. A second view holds that all resin-producing taxa than angiosperms. Extant environments, particularly those of the tropics, gymnosperm resin producers include only two harbor a variety of arthropod herbivores, and prominent lineages—the more southern fungal and other microbial pathogens; hemispheric Araucariaceae, and the northern consequently, plants select for increasing the hemispheric Pinaceae, the latter of which quality and volume of antiherbivore or encompasses the dominant resin producers of antipathogen targeting of host-plant defenses. Pinus (pines), Picea (spruces), Abies (firs), Larix Terpenoid resin flows are a prime example of (larches, tamaracks), and Pseudotsuga (Douglas such defensive capability. Indeed, terpenoid and fir), which inhabit cool temperate zones. other resins, such as phenols, are an ideal and Unfortunately, the Pinaceae produce Class V versatile mechanism to prevent pathogen and resins that do not preserve well in the fossil insect attack through constitutive and induced record. defenses. (Constitutive defenses are baseline A greater diversity of angiosperm taxa are mechanisms that are part of a plants’ normal resin producers when compared to gymnosperms, metabolism; induced defenses are inordinate and mainly occur in tropical to warm-temperate responses that are directly triggered by pathogen localities. On average, each angiosperm species or herbivore attack.) Ironically, volatilized resin produces significantly less amber volumetrically components not only act as deterrents, but also than the average gymnosperm producer. Lesser serve as attractants, particularly involving certain known angiosperm resin producers are the bark- and ambrosia beetles that are enticed toward Clusiaceae (mangosteen family), Euphorbiaceae trunk surfaces (Labandeira et al., 2001). (spurge family), well known for producing rubber, Several lines of evidence suggest against the and the Arecaceae (palm family), containing hypothesis that resin production is only a mucilage exudate and the only monocot resin consequence of plant secondary metabolism. The producer. The better-known resin producers of availability of carbon for terpenoid and other Anacardiaceae (sumac family), Burseraceae, similar bimolecular biosynthesis cannot explain D i p t e r c a r p a c e a e , a n d F a b a c e a e , a r e the dazzling variability in terpenoid molecular overwhelmingly dominant in the Neotropical compounds (Sturgeon, 1979), and the (Fabaceae), west African (Fabaceae, Burseraceae) considerable changes in the volumes of resin a n d e a s t I n d i a n a n d I n d o n e s i a n produced (Tomlin et al., 2000; Klepzig et al., (Dipterocarpaceae) rainforests (Langenheim, 2005). In addition, the broad variety of wood- 1995). These plants have evolved with plant attacking pathogens and arthropod herbivores— herbivores and pollinators, resulting in interesting viruses, wilts, fungal endophytes, white rots, reciprocal adaptations involving resin as a pitch-canker fungi, heartwood borers and resource. The Burseraceae contains pantropical cambium engravers—presently dominate tropical resin-producing Protium and Dacyrodes (safou) and warm-temperate ecosystems (Hillis, 1987; (Cowan and Polhill, 1981), as well as xeric- Pearce, 1996; Labandeira and Prevec, 2014). In adapted Old World genera, such as Boswellia these tropical ecosystems, Hymenaea and (myrrh) and Commiphora (frankincense). The Copaifera have been examined to understand why most copious resin producers are tropical and there are large differences in resin concentration
166 LABANDEIRA: AMBER from various organs of the plant including leaves, fruit, stems, and roots. Langenheim (1984) showed that abiotic factors such as light, soil nutrients, water availability, and climate do not materially explain resin production, whereas biotic factors, such as pathogen colonization and insect herbivory, were responsible not only for high levels of resin production, but also dramatic increases in resin levels immediately after attack (Langenheim et al., 1986). The predilection for high levels of resin production, and hence the ability for self-defense, also is contingent on the presence of particular host-plant clades that have secretory canals and the metabolic machinery to produce latexes, mucilages, gums, and resins (Fahn, 1979). In a study of plant lineages that possess secretory canals but whose sister-group lineages did not, it was found that secretory- canal-bearing lineages had a significantly greater diversity in 13 (69%) of 16 sister-group pairs examined (Farrell et al., 1991). There is a rich fossil record of damage consisting of pith borings, cambium engravings, and heartwood borings throughout the Cenozoic (Guo, 1991; Böcher, 1995; Grimaldi et al., 2000b; Labandeira et al., 2001), Mesozoic (Zhou and Zhang, 1989; Jarzembowski, 1990; Tapanila and Roberts, FIGURE 1.—Amber taphonomy. 1) Resin flows can 2012), and late Paleozoic (Weaver et al., 1997; accumulate in bark fissures and cavities in the wood. Labandeira and Phillips, 2002; Naugolnykh and 2–4) Resin engulfs and traps organisms such as Ponomarenko, 2010). The role of arthropods in insects through entrapment under subaerial inducing resin flow has been suggested for conditions by: 2) drops; 3) stalactites; and 4) flows phytophagous mites in the production of late or subterranean deposits (where resins are produced Triassic cheirolepidiaceous Dolomites Amber in by roots), eventually resulting in entombment of northeastern Italy (Schmidt et al., 2012). A record organisms. 5) In most cases, resins are transported to of needle and leaf mining and feeding defense in sites proximal to their source (allochthonous resin-producing plants has been documented at deposits). 6) In some cases, resins undergo transportation to sites distal to the amber source the tissue (Labandeira, 2013), organ (Labandeira, (parautochthonous deposits) through erosion. (5, 7) 2006), and species (Labandeira, 2002; Wilf et al., Resins encounter a nearby aquatic environment 2006; Lopez-Vaamonde et al., 2006; Schachat et directly from the tree as flotsam. 8) Frequently, al., 2014) levels. In rich amber deposits, there are initial deposition of resin is associated with organic- diverse records of wood-boring beetles such as rich sediments. Where there is significant burial, the bark and ambrosia beetles co-occurring with diagenetic process of amberization begins. 9) Baltic (Schedl, 1947; Larsson, 1978) and Sometimes, these deposits can be recycled into Dominican (Bright and Poinar, 1994) ambers. younger deposits. Modified from Martínez-Delclòs, ! et al. (2004); permission for reproduction granted by THE AMBER PRESERVATIONAL ROUTE Elsevier BV and image kindly provided by Enrique ! Peñalver. The preservation of amber begins with the occurs. The entire process from resin production internal generation and movement of resin on the through eventual unearthing and archiving in an source plant’s external surface. This is followed amber collection continues to the present day by the mechanisms of initial entrapment, then (Fig. 1). subsequent entombment of organic material, and ! eventually ending in transportation of the amber Resin flows clasts to a deposit, where further modification Tree resin is produced in two fundamentally
167 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 different ways. One mechanism is schizogenous (Naugolnykh and Ponomarenko, 2010), it was production, where resin is secreted by specialized during the mid-early Cretaceous that there was a parenchymatous cells that form pools in cavities major volumetric expansion in resin production within the bark, cambia, and wood, and flows to (Molino-Olmedo, 1999; Martínez-Delclòs et al., the bark surface through fissures (Fahn, 1979; 2004). This event coincided with the postulated Mauseth, 1988). A second mode of resin origin and earliest body- and trace-fossil formation is lysogenous production, which occurrences of many xylophagous beetle groups, secretes resin into a system of tubular canals that and the earliest appearance of wood-associated ramify throughout the plant (Mauseth, 1988). As termite sociality (Martínez-Delclòs and Martinell, resin exits the internal environment of a woody 1995). Many of these insect lineages initially trunk or branch, or leaves and roots, it is exposed were associated with the gymnospermous hosts to the external environment as it begins to flow. Araucariaceae, Cheirolepidiaceae, Cupressaceae, Resin movement is dependent on internal sap and Pinaceae (Jarzembowski, 1990; Sequeira and pressure, resin viscosity, ambient temperature, Farrell, 2001; Néraudeau et al., 2002; also see light intensity, and the mass of the descending Ding et al., 2013), some of which were hosted by blob that is providing downward momentum angiosperms after the mid-Cretaceous angiosperm (Martínez-Delclòs et al., 2004). As resin is radiation (Labandeira, 2014). These same beetle exposed to the elements, particularly oxygen, lineages became prominent throughout the radiant solar light, and elevated temperature, there Cenozoic (Labandeira et al., 2001; Martínez- is polymerization of some terpenoid compounds Delclòs et al., 2004), creating conditions for (Whitmore, 1977). Conditions for increased resin profuse resin production by such plants as flow are most optimal in spring to summer in a Hymenaea and Protium. Consequently, the thermally seasonal climate, but may occur during significantly increased production of resin was dry seasons in climates where water availability exacerbated by or even attributable to extensive varies annually. The formation of successive resin tunneling activities into trunk tissues. flows may occur daily, but also may be present on ! a longer term, often seasonal basis, affecting Entrapment especially stalactitic amber masses (Larsson, Once resin flows are present, entrapment 1978). Amber stalactites have distinctive surface ensues. Microorganisms, plants, fungi, laminations that are rich in layered accumulations arthropods, and small vertebrates are the principal of smaller-sized insects as they become attached organisms that are entrapped. The six fundamental to ephemeral sticky surfaces between each factors involved in entrapment that affect renewed flow event (Weitschat and Wichard, arthropods the most are: 1) resin viscosity; 2) 2002). The trapped insects die from asphyxia, and organism behavior; 3) occurrence in particular frequently are overwhelmed by multiple resin habitats; 4) various environmental conditions that flows before they are sealed from the promote resin production; 5) plant defenses; and environment, occasionally undergoing predation, 6) a variety of agents that allow accumulation of disarticulation, and decomposition in the process body parts, such as ant refuse heaps. The (Martínez-Delclòs et al., 2004). These daily to importance of resin viscosity is evident in often seasonal changes in flow determine the taxonomic subtle features attending the incorporation of composition of ambers, and typically record organisms in amber. More viscous resins possess unique combinations of (e.g.) nocturnally versus greater surface tension, which discourages diurnally active insects, aerial pollen maxima for entrapment of small vertebrates, such as geckos, particular plants, and capture of fungal spores and larger, sturdy arthropods, such as centipedes, originating from particular microhabitats, katydids, walkingsticks, and longhorn and scarab especially ephemeral events during the spring and beetles, and also provides the ability of those summer (Richardson et al., 1989; Martín-Delclòs, same insects to struggle free when compared to et al., 2004; Peñalver and Grimaldi, 2006). considerably smaller arthropods (Henwood, Saproxylic beetles consume wood but feed on 1993a). Often a struggle results in self-autopsied fungi, and are a major cause in allowing resin to legs (Néraudeau et al., 2002; Weitschat and flow outward on trunk surfaces. Although wood- Wichard, 2002; Penney, 2005a). In analyses of boring beetles have a record throughout the various amber deposits, large insects are rare; for Triassic (Walker, 1938; Linck, 1949; Tapanila and the Álava Amber from Spain, only 3% of insects Roberts, 2012) and back into the Late Permian are more than 4 mm long (Alonso et al., 2000).
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Insect behavior is another factor in on upper canopy or undergrowth foliage that drop entrapment that favors those insects that land in or into fluidized, mobile resin flows below their are camouflaged by bark, bore into wood or other habitats (Krzemińska et al., 1992). A fourth, hardened tissues, or congregate in soil-surface overrepresented component of insects found in swarms (Koteja, 1996; Poinar and Poinar, 1999). amber are large, winged insects occurring in More specific behaviors associated with particular wetland or other aquatic habitats whose immature insect taxa include resin-foraging bees developmental stages are aquatic, such as (Gonçalves-Alvim, 2001) and termites that shed stoneflies (Plecoptera) and alderflies their wings during nuptial flights, often (Megaloptera), particularly in Siberian Amber accumulating in great numbers (Pike, 1993). (Zherikhin and Sukatcheva, 1990). For Baltic Insect pollinators, such as ginkgoalean pollinating Amber, there is overrepresentation of caddisflies thrips, become entrapped in amber and leave trails (Trichoptera), marsh beetles (Scirtidae), and a of pollen grains as they locomote through plethora of nematocerous flies, particularly relatively non-viscous resin (Peñalver et al., nonbiting midges (Chironomidae) (Weitschat and 2012). Occasionally, aquatic insects possess Wichard, 2002), some of which originated from behaviors that also favor disproportionate phytotelmata such as tank bromeliads (García- entrapment in amber. Certain aquatic beetles, such Gimeno and Peñalver, 2007). The final, perhaps as water scavenger beetles (Hydrophilidae) and nonintuitive, component of amber is underground predaceous diving beetles (Dytiscidae), are soil fauna (Nissenbaum and Horowitz, 1992). Soil disproportionately attracted to fluidized fauna houses oribatid mites, tardigrades, asphaltum with a water-body-like surface sheen springtails, termites, millipedes, earwigs, root- (Horváth and Kriska, 2008), and are over- maggot flies, ants, and small, edaphic beetles represented in brea deposits (Churcher, 1966). (Martínez-Delclòs et al., 2004; Nardi, 2007). The These same groups of insects, as well as muscid presence of in-situ underground amber produced flies and wood-boring beetles, also can be by the roots of long-lived, resin-producing trees attracted visually or chemically to resin pools has been controversial (Martínez-Delclòs et al., with water-like surfaces (Agee and Patterson, 2004). However, evidence from modern 1983; Fatzinger, 1985; Horváth and Kriska, Hymenaea (Henwood, 1993a) and Agathis 2008). These fluid accumulations are excellent (Whitmore, 1980) indicates that a significant resin-pool traps (Szwedo, 2002). accumulation of amber is produced autogenously Insect habitat can have a profound effect in by source-plant roots and litter, and is responsible the taxonomic composition of organisms that for trapping underground biota (Nissenbaum and become trapped in amber. Five principal habitats Horowitz, 1992; Perrichot, 2004). are disproportionately represented in the fossil Plant defenses (mentioned earlier in the amber record. First are bark and wood habitats, context of terpenoids acting as an anti-xylophage which are perhaps the richest single source of mechanism to deter insect attack) also can be an amber inclusions (Poinar and Poinar, 1999). attractant for insects. Resin bugs (Hemiptera: These cortical habitats consist overwhelmingly of Reduviidae), resin-collecting bees (Hymenoptera: beetles, including heartwood borers and cambium Megachilidae, Apidae), bark and ambrosia engravers, but also non-xylophagous animals beetles, and pollinating insects of angiosperm inhabiting the nooks and crannies of bark, resin-producing hosts are attracted to specific or a particularly the interface between the cambium combination of particular volatile terpenoid layer and the frequently partially delaminated molecules, and possibly phenol compounds bark (Larsson, 1978). Bark and wood habitats are (Armbruster, 1984; Fatzinger, 1985; Poinar, associated with patches of moss, lichens, and 1992b, 2010a). The ecological roles that epiphytes nestled in bark interstices, and include terpenoids and associated volatile compounds tardigrades, mites, pseudoscorpions, amphipods, play in alternatively sequestering insects for springtails, and a variety of minute beetles benefits such as pollination, and resisting the (Larsson, 1978). A second important life-mode of deleterious effects of pathogens that are vectored organisms found in amber are small, aerial insects by bark beetles, is a fascinating aspect of the susceptible to wind transport (Martínez-Delclòs et plant‒insect associations of resin-producing trees al., 2004), notably midge-sized nematocerous (Labandeira et al., 2001; Poinar, 2010a). flies, but also smaller-sized insects such as thrips, The important role of environmental factors is parasitoid wasps, and moths. Third are folivores significant for increasing resin production that
169 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 lead to increased rates of organism entrapment. deposits for principally keratin-containing tissues, Radiant solar light, temperature, and water and, to a lesser extent, non-integumentary soft availability are major determinants of resin tissues such as eggshell membrane, muscles, production. For example, Hymenaea courbaril digestive organs, and various cells of Mesozoic growing under conditions of greater water vertebrates (Schweitzer, 2011). A broader variety availability produces more resin than individuals of organs, tissues, and cells from animals, living under water stress (Langenheim, 1967), p r o m i n e n t l y d o c u m e n t e d f r o m leading to more levels of biotal entrapment. penecontemporaneous mid-Eocene deposits at Droughts may have positive indirect effects on Geiseltal (Voigt, 1988) also occur at Messel, in resin production through the fissuring of bark central Germany (Wuttke, 1992), and offer a after major fires that induces resin production and comparison to dipteran flight-muscle tissue in higher volumes of flow for engulfing organisms, Dominican and Baltic ambers. at least for dipterocarp forests in Indonesia Probably the best-preserved documented (Heywood, 1993). Such a scenario also is insect flight muscle in amber is from a dance fly suspected for forests of Juniperus hypnoides (Empididae) in early Miocene Dominican Amber (Cupressaceae), the source plant for New Jersey (~17‒20 Ma; Henwood, 1992a). Muscles are Amber (Grimaldi et al., 2000b; also see Knight et composed of tubular cells of muscle fibers that, in al., 2010), which is associated with abundant turn, consist of elongate contractile proteins, charred remains of plants, coprolites, and insect called myofibrils, which are the basic rod-shaped exoskeletons (Crepet et al., 1991). A possible unit of muscle tissue. After embedding, staining, related environmental factor is soil type, which fixation, and examination under transmission affects resin production through source-tree electron microscopy, the specimen revealed nutrition. Brazilian Copaifera multijuga trees myofibrils (Fig. 2A). Among the myofibrils, growing in clayey soil produce significantly more densely packed mitochondria were identified, resin than conspecifics in sandy soil (Alencar, some of which displayed cristae (Henwood, 1982). 1992a). Although the general conformation of Another factor promoting biotal entrapment empidid flight muscle from Dominican Amber within resin involves the incorporation of exhibits some distortion, attributable to the arthropod fragments and other organic debris entombment process of resin polymerization, it from biological processes of animals. The results displays considerable similarity to modern of spider predation on other arthropods, for dipteran flight muscle from a blow fly example, can result in refuse heaps of discarded (Calliphoridae) (Fig. 2C). The only notable sclerites and other body parts that represent a exception in this comparison is the shrinkage of variety of prey items (Weitschat and Wichard, fossil myofibrils to one-third the size of modern 2002). Other sources of biologically induced dipteran flight-muscle myofibrils, to where they accumulations of organisms incorporated in resin approximate the size of the mitochondria. Other include carcasses associated with spider webs studies of preserved material suggest that similar (Peñalver et al., 2006; Knight et al., 2010), insect preservation of muscle tissue is common coprolites with identifiable dietary contents (Grimaldi et al., 1994). (Néraudeau et al., 2002), and shed exuviae from The flight muscle of the stingless bee molting insects (Kutscher and Koteja, 2000). Proplebeia dominicana (Apidae) was examined ! by Grimaldi et al. (1994) using scanning and Entombment transmission electron microscopy. Their results, Entombment constitutes all of the processes captured in SEM images (Fig. 2D–H), are shown immediately after entrapment and death of an in a less magnified scale than that of Henwood organism or incorporation of an inanimate (1992a), but provide detailed surface views of biological element as it becomes surrounded by individual muscle bundles (Fig. 2D). Under resin, and before the resin loses contact with the transmission electron microscopy (TEM), external environment prior to solidification. The however, longitudinal sections revealed the Z- most consequential process of entombment is band within the myofibrils and the M-band within preservation of soft tissue (Stankiewicz et al., each myofibril. The M-band represents the 1998). The process of modern soft-tissue uncontracted, or relaxed myofibrillar position. preservation has been modeled in the laboratory, Mitochondria also were preserved, seen as and deduced from compression-impression ‘fingerprint’ patterns of parallel, curvilinear
170 LABANDEIRA: AMBER structures under TEM, and better resolved than Gonzales et al., 2009). From the same deposit, those imaged by Henwood (1992a). Although the Speranza et al (2010) used bright-field light mitochondria were not detected in an examination microscopy to document fungal mycelia plastered of decay of modern shrimp in the laboratory, on a thrips’ body, spotlighting internal details of monitoring of muscle phosphatization revealed the hyphae and associated sporangia (Fig. 2I–J). preservation of myofibrils with probable M- and Among the oldest Mesozoic ambers known, Late Z-bands (Briggs and Kear, 1993). This suggests a Triassic Dolomites Amber (~230 Ma) from similar timing for preservation of muscle during northern Italy revealed a variety of protists, fungal phosphatization in compression-impression spores, ensheathed filamentous algae, and other fossils, analogous to early stages of carcass decay microorganisms, some with preserved organellar in resins. contents (Schmidt et al., 2006). Other insect and plant structures from As is the case in other types of preservation, Dominican Amber were imaged under scanning color is very rarely preserved in amber (Martínez- electron microscopy (SEM). These features Delclòs et al., 2004; Thomas et al., 2014). One included pollen lodged on the abdomen of exception is Dominican amber, in which certain Proplebeia dominicana (Fig. 2E), midgut tissues Hemiptera, such a flat bugs (Aradidae) and leaf of a fungus gnat Mycetophila sp. (Diptera: hoppers (Cicadellidae), reveal color patterns Mycetophilidae) (Fig. 2G), the pleated midgut (Poinar, 2010a), as do butterflies (Peñalver and wall of a taxonomically undetermined ambrosia Grimaldi, 2006b). More commonly preserved in beetle (Platypodidae) (Fig. 2H), and columnar amber are grayscale patterns involving darker cells from palisade parenchyma of a Hymenaea versus lighter regions, representing differential protera leaflet (Fig. 2G). Henwood (1992b) also preservation of the melanin pigments in the imaged a sap beetle gut (Nitidulidae), showing the darker, carbonized areas (Poinar, 2010a). Melanin proventricular valve at the posterior end of the pigments have been detected in fungi from lower hindgut that acts as an ancillary triturating device Eocene amber (Beimforde et al., 2011). for transportation of food boluses to the rectum ! (Fig. 2A). Penney (2005a) recorded blood tissue Transportation and deposition exiting the patellar tibial joint in an autopsied Typically, entrapment and entombment last distal-leg segment during amber immersion. from a few hours to a few days (Martínez-Delclòs Dominican Amber has been used the most for et al., 2004), but resin masses can accumulate and histological taphonomic studies, but a few studies remain exposed on the forest ground surface up to have used older ambers. The foliar anatomy of a a few years to perhaps decades (E. Peñalver, pers. cypress twig from Baltic Amber (37‒34 Ma), comm.) before transportation to the immediate about twice the age of Dominican Amber, was site of deposition. Eventual deposition of the resin examined by TEM and light microscopy, showing clasts is a much longer-term process that may take that all elements of vascular, mesophyll, and from weeks to millennia. The prelude to epidermal tissues, and their substructures, were transportation begins with entombment, a nearly identical with extant Chinese swamp preburial process during which inclusions are cypress (Glyptostrobus pensilis, Cupressaceae) preserved amid a variety of internal chemical anatomy (Koller et al., 2005). Using SEM and X- processes. Resin blobs assume a solid form ray computer tomographic techniques, amber preparatory to inclusion as clasts, such as found in from the 65.5 Ma Hell Creek Formation of South Cretaceous amber of Jordan (Nissenbaum and Dakota revealed delicate tissues of internal Horowitz, 1992). The density of resin‒copal‒ organs, such as muscle fibers. Older amber (~101 amber ranges from 1.0–1.3, depending on the Ma), from the lowermost Upper Cretaceous of degree of polymerization and density of the Archingeay-les-Nouillers in northern France, bore transporting medium, resulting in relative ease of exceptional preservation at the organellar level conveyance to a nearby depositional site. With (Girard et al., 2009). In slightly older amber, of rare exceptions, such as Lower Cretaceous amber uppermost early Cretaceous age (~110 Ma) from of Jordan (Nissenbaum and Horowitz, 1992), Álava, Spain, organelles of protists were most amber-bearing deposits are allochthonous preserved as pyrite replacement, indicating accumulations. Transportation from the amber ‘double fossilization’ resulting from an anaerobic source tree to an initial depositional area in a environment in which sulfate-reducing bacteria fluvial, deltaic, lacustrine, or even nearshore- played a major preservational role (Martín- marine environment frequently is from a few to
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172 LABANDEIRA: AMBER tens of kilometers; much less commonly, a few palynodebris may indicate sufficient dispersal hundreds of kilometers (Martínez-Delclòs et al., throughout the sediment such that it did not reach 2004; Girard et al., 2008, 2009). A special levels of detection. By contrast, in a different exception may be lignitic strata that contain study (Gastaldo and Hue, 1992), dipterocarpacean multiple amber deposits, such as some Dominican resins from the Mahakan River delta in Borneo Amber (Penney, 2010a). However, it is more were represented by rounded, large, and variously likely that these deposits were transported shaped cylindrical casts from resin infillings of parautochthonously, close to their source area duct-like networks associated with carbonaceous (Knight et al., 2010), or allochthonously, more plant debris. Interestingly, the Mahakan River distant from their source areas (Martínez-Delclòs delta is a significantly higher-energy system than et al., 2004). On rare occasions, amber is present the Mobile Delta. One explanation accounting for within fossil wood as a result of host-plant this difference in preservation is that resin in the response to beetle borings, and effectively occurs Bornean localities were rapidly deposited whereas in situ (Labandeira et al., 2001). Similarly, amber at the Alabaman sites, resin underwent abrasive may be transported long distances protected from transport for a prolonged period of time. The the elements as ingested gastroliths, as in the case Mahakan River material is analogous to the of an early Cretaceous bird from Lebanon that Peñacerrada II site of Spanish Álava Amber, was found with amber clasts as gut contents which occurs in a coarse-grained sedimentary (Dalla Veccia and Chiappe, 2002). facies (Alonso et al., 2000; Peñalver and Delclòs, Often, amber is not found in deposits where it 2010). may be expected to accumulate, given the The best-studied deposit for transportation of presence of source trees with abundant resin- amber is Baltic Amber. The age of Baltic Amber producing capabilities and suitable nearby is a source of considerable discussion. The oldest environments conducive for preservation. In a recorded date is middle Eocene (Lutetian Stage, study of the Holocene Mobile Delta in Alabama, 44.4 Ma; Ritzkowski, 1999), which probably U.S.A., resin was not found when the plant represents one of the original source deposits. taphonomy and sediments of a backswamp oxbow However, based on exacting stratigraphic studies, were examined (Gastaldo et al., 1987, 1989). Nor the vast majority of original amber comes from did resin occur in a crevasse splay associated with deposits of 37–34 Ma (Standke, 1998, 2008), and an extensive presence of resiniferous bald is late Eocene in age (Priabonian Stage). cypress, Taxodium distichum (Cupressaceae). The Nevertheless, Baltic Amber is found in younger lack of discovery may be attributable to physical deposits throughout northern Europe along destruction of resin soon after it was produced, coastlines of the Baltic Sea (Larsson, 1978; not far from its source. Alternatively, the Weitschat and Wichard, 2002). The source zone of fragmentary, microscopic nature of the resin as Priabonian-age Baltic Amber, the Blaue Erde
←FIGURE 2.—Preservation potential of amber at tissue level shown from microscope sections and scanning electron micrograph (SEM) images of anatomical dissections from insect inclusions in early Miocene Dominican Amber of the Dominican Republic (A, B, D‒H), and bright-field microscope images from Álava Amber, Spain (I‒ J). A) Proventriculus region of the foregut from a nitidulid beetle (Henwood 1992b, fig. 3, specimen SM X. 23254). B) A transmission electron micrograph in transverse section of flight muscle of a dance fly (Diptera: Empididae) (Henwood 1992a, fig. 3; MF=myofibrils; M=mitochondria; arrow=mitochondrial cristae). C) Analogous structures to (B), showing a transmission electron micrograph of modern fly flight muscle (Diptera: Cyclorrhapha) from the blow fly Calliphora vomitoria (Henwood 1992a, fig. 2; MF=myofibrils; M=mitochondria). D) SEM of a thoracic muscle bundle with transverse striae of the stingless bee, Proplebeia dominicana (Grimaldi et al., 1994; fig. 10). E) SEM of a pollen cluster retrieved from the abdomen of the stingless bee Proplebeia dominicana (Grimaldi et al., 1994; fig. 13). F). SEM of the opening to the proventriculus from the fungus gnat Mycetophila sp. (Diptera: Mycetophilidae) (Grimaldi et al., 1994; fig. 21). G). SEM showing a stack of columnar palisade cells from a leaf, probably Hymenaea protera (Grimaldi et al., 1994: fig. 45). H). SEM of deeply pleated microstructure lining the wall of the ventriculus of an unnamed platypodid beetle (Grimaldi et al., 1994; fig. 39). I). Fungal hyphae overgrowing an entombed thrips specimen (Speranza et al., 2010; fig. 3b). J). Fungal mycelial mat, with individual hyphae indicated by arrows (Speranza et al., 2010; fig. 6a). Figures without specimen numbers indicate that they were not provided in the original publication or were destructively analyzed. Scale bars: vertically lined=10 µm; horizontally lined=100 µm. (A–C) Reproduction courtesy of the Palaeontological Association. (D–H) Reproduction courtesy of the American Museum of Natural History. (I–J) Reproduced with permission courtesy of the Formatex Research Center.
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(‘Blue Earth’) strata, is particularly productive in promoted by inclusion-associated bacteria and the Samland Peninsula, near Kaliningrad, Russia resulting in mummification of tissue (Henwood, (Kosmowska-Ceranowicz, 1996). However, older 1992a, 1992b). Perfusion of terpenoid compounds Baltic Amber was recycled in subsequent, into the inclusion probably enhances the younger deposits (Weitschat and Wichard, 2002), preservation process (Grimaldi et al., 1994). in which the same arthropod species of Baltic During the early phase of amberization, Amber occur. These younger ambers include the production of the whitish cottony covering late Eocene Rovno Amber of Ukraine (Perkovsky mentioned above may be caused by the et al., 2010), latest Oligocene to earliest Miocene production of milky-appearing fluids, resulting in Bitterfeld Amber (Dunlop, 2010), Pleistocene degassing of very minute bubbles. This glacial deposits (Neubauer, 1994), and, during the production is especially prominent for larger Holocene and today, in numerous sandy and invertebrates with an excess of soft tissues, such clayey littoral deposits along the Baltic Sea and as insect larvae, making viewing very difficult. its adjacent bays (Weitschat and Wichard, 2002). Carbonization affects structures such as cuticle, These Baltic Amber-bearing deposits indicate at which are transformed into carbon-enriched, least four cycles of sedimentary exhumation and linear-chain hydrocarbons and aliphatic polymers redeposition of amber. (Stankiewicz et al, 1998). ! Amberization also includes longer-term Amberization physical processes after amber clasts have been The beginning of diagenesis of resin consists incorporated in a sedimentary deposit. Depending of two processes within a tree-resin blob as an on membership of an amber clast in one of the insect becomes engulfed. The first process is five compositional classes of amber, and its short-term, and involves the effects of organisms access to the atmosphere, amber will oxidize that are embedded within the resin, which along the periphery of the clast, particularly upon commences with entrapment (Martínez-Delclòs et exhumation (Grimaldi et al., 2000a). This process al., 2004). Resin terpenoids are laden with various causes a darkening in color, typically from a antiseptic and antimicrobial compounds that often yellow to a darker red (Martínez-Delclòs et al., protect the insect body from decomposition by 2004), resulting in formation of a noticeable rind. saprobic microorganisms and fungi (Langenheim, In addition, exposure of amber to variable 1990). In some instances, however, amber humidity, elevated temperature, and high light inclusions, particularly insects, display a whitish levels will produce surface cracking, or crazing to light yellowish, cottony fungal coating, (Bisulca et al., 2012). Older Cretaceous ambers presumably a mycelial mat (Henderickx et al., are more susceptible to deterioration than 2006, 2013; Peñalver and Delclòs, 2010), that Neogene ambers. suggests a lack of effective amber fungicidal The role of the rock overburden is important properties during late entrapment and early for diagenetic processes. Extensive entombment. Such a fungal coating of the polymerization of amber, facilitated by external body surface indicates that the fungus considerable sediment load, causes amber clasts grew immediately after entrapment, sometimes to become brittle and deformed. The lessening of into the resin itself and onto the carcass surface overburden pressure often induces microscopic (E. Peñalver, pers. comm.), but before the cracks between the inclusion and the outer margin perfusion of resin through the inner tissues of the of the enveloping amber, causing circumferential inclusion and hardening of the resin. An cracks and haloes surrounding the specimen. alternative hypothesis is that the whitish covering Under very high temperatures, amber may is not fungi at all, but rather an emulsion of become flattened, bidirectionally deformed, and microscopic bubbles that avoided direct sunlight, melt (Grimaldi, 1995; Zherikhin and Eskov, which is responsible for resin clarity and 1999). elimination of the bubble cloud (Schlüter and Weathering is a process destructive to amber, Kühne, 1975). principally through oxidation, but also by Other short-term, major changes to the exposure to fluctuating physical variables such as inclusions are dehydration and carbonization, the diurnal cycle of light intensity, temperature, which also begin with entrapment (Martínez- and humidity. Weathering imparts a brittle, micro- Delclòs et al., 2004). Dehydration limits the fissured outer layer (crazing) to amber clasts that natural processes of autolysis (tissue degradation), increases deterioration through time. Minerals
174 LABANDEIRA: AMBER such as pyrite may gain entry into the amber clast of ~540 arthropod families, and Dominican and form crystalline infillings of cracks along the Amber comprised of ~300 arthropod families. outer rind (Baroni-Urbani and Graeser, 1987). These two deposits provide the best examples in Penetration by pyrite may extend to the outer the fossil record for understanding the complexity surfaces of inclusions from microorganisms or of foodweb structure and the intricateness of arthropods, representing secondary mineralization inter-organismic activity. (Schlüter and Stürmer, 1982; Martín-Gonzalez et ! al., 2009). In very rare instances, the tissues of an Phase 1 entirely entombed insect may be replaced with The first phase involves the earliest deposits pyrite (Schlüter, 1989). of amber in the fossil record that involves three ! major occurrences (Fig. 3; Table 1). The earliest MAJOR FEATURES OF THE AMBER appearances of amber are from early RECORD Pennsylvanian to late Permian Euramerican ! deposits that are attributed to extinct early seed The fossil record of amber can be divided into plants—a medullosan and a cordaite. The four major phases. These four phases provide a terpenoid-based amber chemically analyzed from temporal context to the 25 most significant amber these paleobotanical sources apparently has no deposits (Table 1,
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FIGURE 3.—Paleozoic amber consists of resin rodlets in medullosan trunks (which also occurs rarely in modern conifers). A) Digital photograph of acetate peel 39875A of Myeloxylon, a medullosan trunk (Herrin Coal, Carbondale Formation, Middle Pennsylvanian, from the Peabody Eagle Surface Mine, Shawneetown, Illinois); black arrow indicates position of resin canals and resin rodlets within the trunk; peel is ~25 cm long (University of Illinois Urbana-Champaign Ecological Studies peel 39875A). B) Enlarged photograph of Late Pennsylvanian Myeloxylon trunk (Calhoun Coal, Mattoon Formation, Berryville, Illinois); transversely cut trunk ~2 cm long with darker-hued structural tissues amid smaller mucilage or resin canals, as indicated by the arrow (United States National Museum peel BV37-Gbot, microscope slide 110). C) A near-transverse section of a resin rodlet showing internal vesicles (late Pennsylvanian Danville Coal, Illinois; from Kosanke and Harrison, 1957, pl. 1, fig. 2, x900). D) Isolated, partly fusanized resin rodlets macerated from the Herrin Coal (Kosanke and Harrison, 1957; fig. 5; longest specimen is ~10 mm). E) A partly fusanized resin rodlet in oblique longitudinal section. (Kosanke and Harrison, 1957, fig. 6, x300). F). A fragment of the earliest-known amber (arrow indicates border of specimen) from a coal in the Tradewater Formation, Middle Pennsylvanian, Illinois. This specimen was determined to be amber by analysis with pyrolysis gas chromatography mass spectrometry. (Bray and Anderson, 2009, fig. 2). Figures without specimen numbers indicate that they were not provided in the original publication or possibly were destructively analyzed. Scale bars: crosshatched=10 mm; solid=1 mm. (C–E) ©1957 University of Illinois Board of Trustees, reproduced courtesy of the Illinois State Geological Survey. tissues (Langenheim, 1990; Weaver et al., 1997; second expansion comes from conifers, such as Naugolnykh and Ponomarenko, 2010), attributed Agathoxylon logs of the Araucariaceae (kauri, to the adult and larval activities of archostematan monkey-puzzle trees and wollemi pine) (Litwin Coleoptera, the reticulated beetles (Cupedidae) and Ash, 1991), the Cheirolepidiaceae (Roghi et and their Permian relatives. These occurrences al., 2006; Schmidt et al., 2012), and probably the lack definitive body-fossil evidence associating Voltziaceae (Labandeira, 2006). Amber was more galleries and tunnels with particular beetle taxa. copiously produced than during the late However, towards the end of the Permian, various Paleozoic, and occurs as significant woods exhibit a significant increase in the accumulations of teardrop-shaped clasts affiliated activities of new wood-boring beetle lineages. with the Cheirolepidiaceae, such as Pagiophyllum ! and Brachyphyllum, often in lignitic strata or Phase 2 associated lag deposits (Fig. 4A–F) (Schmidt et The second phase is the expansion of new, al., 2012). Other occurrences are associated with resin-producing plant clades during the late Agathoxylon logs (Litwin and Ash, 1991), or as Triassic, which continued into the mid- amber replacement of the vacuities that resulted Cretaceous. Plant taxa representative of the from the consumption of ovulate tissue by an
176 LABANDEIRA: AMBER unknown seed predator (Labandeira, 2006) in (Albian, Spain; Fig. 4J–N), Myanmar Amber woody seeds of the probable voltzialean conifer (uppermost Albian to lowermost Cenomanian, Dordrechtites (Anderson and Anderson, 2003). Myanmar), Charentes Amber (Albian‒ The greater prevalence of amber in a variety of Cenomanian boundary, France), New Jersey mostly fine-grained deposits continued until the Amber (Turonian, New Jersey), and Canadian late Jurassic at ~145 Ma, as evidenced by several Amber (Campanian, Alberta and Manitoba) deposits with more substantial amber clasts in the (Table 1). In addition, it is during the third phase range of 5 cm (Grimaldi, 1996; Philippe et al., in which mid-rank Polyphaga beetle lineages 2005; Azar et al., 2010) (Fig. 4G–I). A likely originate and diversify, as evidenced by the early cause for the volumetric increase in amber when diversification of the Cerambycidae (longhorn compared to Paleozoic occurrences was the beetles) and the diverse lineages of the response of conifer trees to the activities of new Curculionoidea, including the Brentidae (straight- wood-boring beetle lineages, including the snouted weevils), Curculionidae (common plesiomorphic symphytan lineages of woodwasps weevils), Scolytinae (bark beetles), and (Xiphydriidae), horntails (Siricidae), and, later, Platypodidae (ambrosia beetles). The response of stem sawflies (Cephidae) (Rasnitsyn, 1980; trees to beetle attack frequently involved Vilhelmsen and Turrisi, 2011). The more basal infective, pathogenic microorganisms that were and plesiomorphic archostematan beetles vectored by a wood-boring beetle, indicated by eventually were ecologically eclipsed by early- to common tree-host signs such as extensive mid-rank polyphagan lineages, such as the production of pitch and resin (Paine et al., 1997). Buprestidae (metallic wood-boring beetles), Evidence for the presence of damage attributable Bostrichidae (powderpost beetles), Anobiidae to bark beetles (e.g., Solomon, 1995), other (deathwatch beetles), and Lymexylidae (timber beetles with bark-beetle habits (e.g., Kuschel, beetles). These hymenopteran and coleopteran 1966), or ambrosia beetles commences during the lineages continue to the present day (Crowson, Early Cretaceous, based on beetle galleries 1981; Solomon, 1995), even as new lineages of (Jarzembowski, 1990), body fossils (Kirejtshuk et arborescent gymnosperms and angiosperms have al., 2009), and the time of origin of the Scolytinae largely replaced preceding phases, often and Platypodinae (McKenna et al., 2009; Jordal et associated with increased amber production. al., 2011; but see Franz and Engel, 2010). In ! addition, anobine beetles of the Ptiniidae are also Phase 3 known from Early Cretaceous ambers (Peris et al., The third phase of the amber fossil record 2014). began just before or during the initial angiosperm ! expansion. However, angiosperms do not become Phase 4 significant resin producers until the fourth phase, The beginning of the fourth phase of amber in the Cenozoic. The predominant third-phase production occurred as a new group of trees are pinalean conifers, particularly the angiosperms—resin-producing taxa that were Cupressaceae (cypresses, junipers, swamp inconspicuous during the late Cretaceous— cypresses, and redwoods), and the Pinaceae became prominent during the Cenozoic. Phase (pines, spruces, firs, larches, cedars, hemlocks, four starts immediately after the K–Pg boundary, and Douglas fir), although earlier resin producers combining gymnosperm resin producers such as such as the Araucariaceae and Cheirolepidiaceae the Araucariaceae, Cupressaceae, and especially were occasional resin producers, particularly the Pinaceae with newly emerging, but rare during the Cretaceous. During the third phase, woody dicot lineages. Amber deposits from there appears to be a significant increase in the angiosperms are very rare during the 35 million quantity of resin produced and in the chemical years of the Upper Cretaceous, perhaps a compositional diversity of resins. This increase is consequence of the paucity of woodiness and reflected in a major mid-early Cretaceous arborescence, or possibly because of being boundary of amber production, marked by the overshadowed by longer-lived and much earlier- onset of Lebanese Amber, during which deposits appearing resin-producing gymnosperm lineages consisted of greater amounts amber than seen in that may have been more effective in resisting the earlier fossil record. The trend established by insect pests. During the Paleogene, the Lebanese Amber continues during the Cretaceous, appearance of the Dipterocarpaceae (Shorea, with subsequent major deposits of Álava Amber meranti), Combretaceae (Terminalia, Indian
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178 LABANDEIRA: AMBER almond), and Hamamelidaceae (Liquidambar) by a greater frequency of amber deposits and a were the earliest angiosperms providing amber in volumetric increase in the amount of amber per sufficiently large amounts to be recognized in the deposit, likely attributable to a greater diversity fossil record. However, the deposit with the wood-boring beetle and sawfly lineages and the greatest diversity and abundance, Baltic Amber addition of new dipteran and lepidopteran wood- (Fig. 5), was mainly produced by conifers, but boring clades. During the Paleogene, the wood- also included angiosperm resins (Anderson and boring niche was invaded by the Diptera (true LePage, 1995; Wolfe et al., 2009; Weitschat and flies), particularly the Agromyzidae (leafmining Wichard, 2010). By contrast, during the Neogene, flies) that attack tree cambium tissue, and the amber production assumed a different character, Panthophthalmidae (panthophthalmid flies) that with source plants dominantly consisting of bore into the trunk heartwood. The Lepidoptera woody shrubs and trees of the Fabaceae, represent a more extensive invasion of indurated particularly Hymenaea, as a major source of resin tissues, and included the frequently large in deposits such as Miocene Dominican (Fig. 6) xyophagous larvae of the Sesiidae (clearwing and Mexican ambers (Penney, 2010a; Solórzano moths), Momphidae (mompha moths), Cossidae Kraemer, 2010) and Pliocene to Holocene (carpenterworm moths), Argresthidae subfossil copal from Colombia, Tanzania, and (argresthiids), Noctuidae (owlet moths), and Madagascar (Schlüter and Gnielinski, 1980; Pyralidae (snout moths), many of which occur in Penney and Preziosi, 2010). Sometime during the twigs and small stems of smaller woody shrubs, mid-Cretaceous to early Paleogene, but varying in and to a lesser extent, the branchlets of larger time and place, there was a general supplement of trees. Individual resin production induced by Mesozoic gymnosperm lineages by angiosperms, shrubs and more modestly statured arborescent some of which may have been caused by the trees was less important in producing larger transfer of life-habits of insect lineages from volumes of amber than were more massive gymnosperms to angiosperms, paralleling a gymnosperm and angiosperm trees that were similar, earlier global host shift during the mid- much more prolific in amber production from the Cretaceous in insect herbivores and pollinators induction of polyphagan beetles, particularly (Labandeira, 2014). This phase was accompanied common weevils, bark beetles, and ambrosia
← FIGURE 4.—Mesozoic amber: Triassic (A‒F), Jurassic (G‒I), and Cretaceous (J‒R) occurrences. A) Outcrop of Triassic (Carnian) Heiligkreuz Formation, Dolomite Mountains near Cortina, Italy, where specimens figured in B‒ F were collected. (Photo courtesy of Eugenio Ragazzi, University of Padova, Italy) B) Typical appearance of amber material attributed to a cheirolepidiaceous conifer (Schmidt et al., 2012; fig. S1). C) Representative amber droplets (Schmidt et al., 2012; fig. 1F, specimen DGPGP-ER-527). D) Disarticulated elements of a nematoceran fly (Schmidt et al., 2012; figs. 1G, and S2, S6; specimen MGP-31345). E) A phytophagous eriophyoid mite, Triasacarus fedelei, a possible galler (Schmidt et al., 2012; fig. 2C, specimen MGP-31343). F) Phytophagous eriophyoid mite Ampezzoa triassica, a probable external leaf feeder (Schmidt et al., 2012; fig. 3A; specimen MGP-31344). G). A rounded amber clast (arrow) of probable cupressaceous origin, Late Jurassic (Oxfordian) of Russia, surrounded by Metasequoia sp. foliage (Grimaldi, 1996). H) Another ovoidal shaped amber bleb (arrow) of Beit Mounzer, Caza District, northern Lebanon (Azar et al., 2010; fig. 2b). I) A parautochthonous amber clast within clayey siltstone of the Khlong Min Formation, Krabi Province, Thailand (Philippe et al., 2005; fig. 3). J–N) Álava amber (Peñacerrada I), Escucha Formation, Spain; J) Early Cretaceous (Albian) elcanid orthopteran, Hispanelcana arilloi (Peñalver and Grimaldi, 2010; fig. 6.3; specimen MCNA-9588); K) Ginkgophyte-pollinating thrips, Gymnopollisthrips minor, with black arrow showing clumps of pollen attached to specialized ring setae (Peñalver et al., 2012; fig. 1B, specimen MCNA-10731). L) An indeterminate species of thrips (Peñalver and Delclòs, 2010; fig. 18E). M) Serphitid wasp Aposerphites angustus (Ortega-Blanco et al., 2011: fig. 3B, specimen MCNA-8651). N) Evaniid wasp Iberoevania roblesi, a likely parasitoid of cockroach egg cases (Peñalver et al. 2010; fig. 11a, specimen MCNA-8759). O) A dichotomously branching actinomycete colony in amber within lignitic clay from Archingeay-Les Nouillers and Cadeuil, late Albian, France (Girard et al., 2009; fig. 1C, specimen ARC-115.22a). P) From the Cadeuil locality, a green alga very similar to Enallax (Girard et al., 2009: fig. 2H; specimen ARC-CDL-26c). Q-R) From the Archingeay-Les Nouillers locality. Q) a testate amoeba very similar to Centropyxis discoides (Girard et al., 2009; fig. 2I, specimen ARC-115.21). R) Spinose sponge spicule with a central canal (Girard et al., 2009; fig. 3E; specimen ARC-115.12c). Figures without specimen numbers indicate that they were not provided in the original publication or possibly were destructively analyzed. Scale bars: solid=1 mm; dotted=0.1 mm; vertical=10 µm; horizontal=100 µm. Permission for reproduction of B–F, K granted by the National Academy of Sciences, U.S.A.. Permission for reproduction of I–J, M granted by Elsevier B.V.
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FIGURE 5.—Plants and arthropods in Paleogene Baltic amber from the early middle Eocene of northern Europe. A) Resin drop within an amber clast. B) Arborvitae branchlet (Pinales: Cupressaceae). C) Early Miocene bryozoan lattice network covering an amber clast. D) Predaceous whirligig mite (Acari: Anystidae). E) Assassin spider →
180 LABANDEIRA: AMBER beetles. Notably, several modern sources of resin display particular interactions of herbivory, that are colonized and attacked by wood-boring parasitism, pathogen-mediated disease, insects are very rare or uncommon in the amber parasitoidism, predation, phoretic associations, fossil record, including the Burseraceae, pollination, and mimicry. Camouflage is another Anacardiaceae (cashew family), and association that has a record (Pérez-de-la-Funte, Combretaceae (Langenheim, 1990). 2012), but will not be discussed herein. ! Amber also presents evidence for interactions INTER-ORGANISM INTERACTIONS that involve special, spatiotemporally ephemeral ! microhabitats such as bark and wood, carrion, One valuable archive of the amber fossil record is dung, polypores and other macrofungal bodies, the primary documentation it provides of the phytotelmata, and resin substrates. The greatest interactions among organisms, such as feeding, number of interactions documented in amber dispersal, and mimicry. Although these data have involve parasites and parasitoids, which differs not been fully exploited, amber deposits are ideal significantly from the dominance of herbivory in for examining ecological structure within a the compression-impression fossil record diverse community. For example, the compilation (Labandeira, 2002). Virtually all important amber of food-web data using deposits such as deposits have evidence that supports a variety of Dominican and Baltic Amber, could surpass that interspecific interactions, with Neogene of the Messel food web (Dunne et al., 2014; Dominican Amber expressing the greatest number Labandeira and Dunne, 2014), which is the most of documented interactions (Poinar, 2010a; well-resolved so far in the fossil record. Of Boucot and Poinar, 2010), followed by Paleogene interest to ethologists is the information that Baltic Amber (Larsson, 1978; Weitschat and amber deposits can provide for intraspecific Wichard, 2002; Boucot and Poinar, 2010), then interactions, such as the reproductive behaviors of Myanmar Amber of the Lower‒Upper Cretaceous mating and lekking. (Lekking is the process boundary (Santiago-Blay et al., 2005; Boucot and where males congregate during the mating season Poinar, 2010; Shi et al., 2013). Levels of to engage in behaviors that attract conspecific documentation among all amber deposits likely is females.) a consequence of 1) the intrinsic biological ! richness of the deposit studied, 2) amber Interspecific interactions preservational state, 3) the availability of material The entire terrestrial spectrum of modern to study, and 4) investigator interest. interspecific interactions is represented in the Phytophages.—The amber record of amber fossil record, characterized by herbivory is far exceeded by the compression- antagonisms, commensalisms, and mutualisms. A impression fossil record. Evidence for herbivory broad representation of major terrestrial groups in the amber fossil record is sparse, but very consists of a diverse menagerie of rarely is there evidence of a direct interaction, microorganisms, fungi, plants, and animals. In such as coccids feeding on a conifer foliage particular, the amber fossil record includes (Grimaldi et al., 2000b). This sparseness is evidence for the presence of viruses; body fossils attributable to the absence of substantial expanses of bacteria; protists, especially protozoans and of two-dimensional surfaces in the permineralized algae; deuteromycete, ascomycete and record, including amber, which would be essential basidiomycete fungi; nematodes; tardigrades; for statistically robust sampling of herbivory on onychophorans; arthropods such as crustaceans, foliage. Nevertheless, there is good evidence for myriapods, arachnids, and hexapods; and small some types of external foliage feeding on a very vertebrates. Species from these organismic groups few, selected species in amber, such as leaves of
← FIGURE 5.—continued. (Araneae: Archaeidae) with extremely long raptorial chelicerae (arrow). F). Dwarf sheet spider (Araneae: Hahniidae) with six spinnerets arranged in a transverse row (arrow). G). Jumping spider (Araneae: Salticidae) with four pairs of eyes (and presumably extremely acute vision). H). Webspinner (Insecta: Embioptera) with a pair of cerci at the abdominal tip. I). Germaraphis baltica (Hemiptera: Aphidae), a member of an extinct lineage of aphids bearing a prominent, elongate ovipositor emerging from the ventral abdominal midsection (arrow). J) Biting midge (Diptera: Ceratopogonidae) showing piercing-and-sucking mouthparts for blood feeding (arrow). K) A small-headed fly (Diptera: Acroceridae) displaying a large, humped thorax at upper right and left (arrow). L) The social insect Electrapis sp. (Hymenoptera: Electrapidae), a member of a major, extinct, bee pollinator lineage. Images contributed by Patrick Craig; scale bars not provided.
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Hymenaea protera in Dominican Amber and the amber record is its record of relationships with possibly H. mexicana in Chiapas Amber. other organisms of the dominant pathogen groups Interactions such as margin feeding, hole-feeding, —viruses, bacteria, fungi, and nematodes (Table and skeletonization are recorded in the Dominican 2, Poinar, 2014). The amber fossil record of Amber record: occasionally interesting herbivory pathogen, vector, and host diversity is exceeded occurs, such as florivory on a Hymenaea flower only by the record of plant-arthropod interactions petal (Solórzano Kramer, 2010; Boucot and from compression-impression deposits Poinar, 2010), sometimes attributable to the (Labandeira et al., 2007). special way that amber preserves leaves. Another Pathogens.—Twenty examples of diseases type of herbivory evidence is recognizable in recorded in amber are detailed in Table 2 (
← FIGURE 6.—Plants, arthropods, and vertebrates in Neogene Dominican amber, early Miocene, Dominican Republic. A) Catkin (male flower) of oak (Fagaceae: Quercus), showing five projecting anthers. B) A hard tick (Acari: Ixodidae) with a prominent, forwardly directed head process (capitulum). C) A swarm of termites (Isoptera: Termitidae) with wings still attached from a nuptial flight. D) Ant (Hymenoptera: Formicidae) trapped in a spider web; note gaseous emissions from the rectum. E) Wood-boring powderpost beetle (Coleoptera: Anobiidae) at bottom; unidentified mite at center (tiny specimen), and a parasitoid scelionid wasp (Hymenoptera: Scelionidae) at top. F). A marsupial and rodent flea (Siphonaptera: Rhopalopsyllidae) displaying piercing-and- sucking mouthparts (arrow) and spinose hindlegs and terminal claws for attaching to the pelage of its mammal host. G) Mosquito (Diptera: Culicidae) head and mouthparts, stylet assembly protruding at lower left (arrow). H) Pupal case of a wood gnat (Diptera: Anisopodidae), showing mandibles in the head section at right. I) A phoretic Leptus sp. mite (Acari: Erythraeidae) latched to the abdominal terminus (arrow) of a long-legged fly host (Diptera: Dolichopodidae). J) Copulating moth flies (Diptera: Psychodidae) with male and female genitalia in a locked position (arrow). K) Two long-legged flies (Diptera: Dolichopodidae) prepositioned for copulation. L) The pollinator bee Proplebeia dominicana (Hymenoptera: Apidae) with orchid pollinia (arrow) enveloping its body. M) The manus of a rain frog, Eleutherodactylus (Anura: Eleutherodactylidae), a consumer of invertebrates, particularly insects. N) Contour feather of a woodpecker (Piciformes: Picidae). O) An egg of a hummingbird (Apodiformes: Trochilidae), a nectar feeder on flowers with deep-throated corollas. Images contributed by Patrick Craig; scale bars not provided.
183 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 amber (Poinar and Telford, 2005) require and specialized adhesive structures that ensnare considerable caution and lack convincing small arthropods for eventual consumption evidence that disease transmission was present. (Schmidt et al., 2008). Amber examples of active Of considerably more recent vintage is the predation appear to be less frequent than Dominican Amber anopheline mosquito occurrences of parasitism and parasitoidism, at Anopheles sp. (Diptera: Culicidae), which is least in the documented record. A recurring closely related to modern malaria-vectoring pattern suggests that the attachment of a species and shares the same, distinctive specialized parasite or parasitoid to their hosts is a anopheline egg type with float structures behavior more readily captured by amber flows (Zavortink and Poinar, 2000). From the same than weaker, more generalized interactions from deposit, another culicid mosquito, the culicine predators and their prey. Culex malariger, possibly housed developmental Phoretic associations.—Numerous examples stages, including oöcysts and sporozonites, of the of phoretic associations occur in all of the major malarial parasite, Plasmodium dominicana, amber deposits, extending to the mid-Early indicating an avian host (Table 2, entry 10; Cretaceous (Boucot and Poinar, 2010). Most Poinar, 2005b), representing a third, inconclusive common are small and often inconspicuous mites, study. More compelling, and with clear contextual pseudoscorpions, and collembolans, which are and associational evidence, is a case from attached to the body surfaces of much larger Dominican Amber wherein there is blood-feeding transporting arthropods (Fig. 6I). Phoretic by five species of Lutzomyia, phlebotomine sand erythraeid, macrochelid, and astigmatid mites flies, one of which was associated with the hair of provide interactions that can best be considered an unknown solenodon (Mammalia: Insectivora), commensalisms, and these mites have latched and probably was involved in the transmission of onto springtails, biting midges, crane flies, Leishmania (Peñalver and Grimaldi, 2006b). An pomace flies, and ambrosia beetles (Poinar, important aspect of excellent amber preservation 1992a, 2010a; Dunlop et al., 2012). Small is the detection of not only suspect disease vectors pseudoscorpions frequently are attached to the on their hosts, but also possible elucidation of the legs, wings, and other appendages of other larger structure at high magnification of miniscule arthropods, such as long-legged flies disease pathogens (Boucot and Poinar, 2010; (Dolichopodidae), snipe flies (Rhagionidae), bark Poinar, 2014), which nevertheless are very beetles, ambrosia beetles, braconid wasps, and difficult to demonstrate, as are the pathological harvestmen (Opiliones) (Grimaldi, 1996; effects of viruses or fossils of bacteria, fungi, Weitschat and Wichard, 2002; Boucot and Poinar, nematodes or other inconspicuous invertebrates 2010). Smithurinid springtails (Collembola) also (Labandeira and Prevec, 2014). have phoretic associations with mayflies and Predators.—Predators are well-represented in harvestmen (Boucot and Poinar, 2010; Penney et amber, some of which were trapped while al., 2012a), an association that has not been pursuing partially engulfed or dangling prey. recorded with modern springtails, unlike those Arachnids frequently are found in the presence of d o c u m e n t e d f o r m o d e r n m i t e s a n d prey, such as arthropods entangled in spider webs pseudoscorpions. The more common phoretic (Peñalver et al., 2006; Knight et al., 2010), a species do not appear to repeatedly target the pseudoscorpion and ant in combat (Poinar, 2001), same host species, indicating that most phoretic or a whipscorpion with prey clutched in its associations have generalist hosts. mouthparts (Grimaldi, 1996). Insect predation Pollinators.—Evidence for insect pollination caught-in-the-act occasionally occurs, consisting from compression-impression deposits of predators that still are grasping or otherwise considerably predates the earliest abundant amber associated with feeding and can be considered deposits of the mid-early Cretaceous (Ren et al., ‘frozen behavior’ (Boucot and Poinar, 2010). 2009; Labandeira, 2010). However, there are Examples include a dance fly with a nonbiting examples of this early, mid-Mesozoic phase of midge enveloped by its legs, an insect larva pollinator history in early Cretaceous amber consuming the head of a scuttle fly, and a praying deposits that document mutualisms between mantis attacked by ants (Grimaldi, 1996; Janzen, insect-pollinated gymnosperms and more basal 2002). An atypical example of predation is the lineages of modern pollinator groups (Labandeira, predatory fungus Palaeoanellus dimorphus from 2010, 2014). One such example is Libanorhinus late Albian French amber that bears hyphal rings succineus (Kuschel and Poinar, 1993), a pine-
184 LABANDEIRA: AMBER flower snout weevil (Coleoptera: Nemonychidae), taxa are efficient pollinators. In significantly an early member of a lineage of weevils that younger Dominican Amber, (~17 Ma), two currently feed on pollen and other tissues from associations stand out. First is the stingless bee c o n i f e r s , p a r t i c u l a r l y A r a u c a r i a c e a e , Proplebeia dominicana (Fig. 6L), with one Podocarpaceae, and Pinaceae (Labandeira, 2002). specimen covered by pollen-containing pollinaria This weevil occurs in Lebanese Amber, at ~120 of a Meliorchis orchid, indicating a considerably Ma, and likely fed on tissues and pollinated older relationship between Neotropical stingless Agathis (Araucariaceae), the principal resin bees and orchids (Ramírez et al., 2007). A second producer for Lebanese Amber. In the slightly association is one of the most heavily studied and younger Álava Amber of Spain (~110 Ma), iconic of pollination mutualisms: figs (Ficus) and another, but very different, gymnosperm-insect fig wasps from various taxa from the Agaonidae pollinator system involved a ginkgoalean-thrips (Hymenoptera). The fig-fig wasp pollinator mutualism, and revealed evidence for pollination mutualism was established by the early Miocene aided by specialized ring setae occurring on the in Hispaniola (Peñalver et al., 2006), although the thrips wings and abdomen with adherent clumps relationship probably began in the Neotropics of Cycadopites pollen (Fig. 4K) (Peñalver et al., much earlier at ~34 Ma, based on molecular 2012). In still younger Myanmar Amber (100 phylogenetic data (Compton et al., 2010). Ma), the earliest-known bee has several features Mimicry.—Examples of mimicry are rare in such as branched hairs, deeply tridentate the amber fossil record. In most instances where mandibles, and anterior abdominal tubercles, color-based mimicry is suspected, pigmentation indicating that there was interaction with the color is obliterated (but see Beimforde et al., reproductive organs of a seed plant, possibly an 2011). In other instances, structural colors are angiosperm. From the same deposit, mosquito- well preserved (Weitschat and Wichard, 2002; sized pseudopolycentropodid scorpionflies plate 75). Perhaps the best example of mimicry (Mecoptera) appear to have a similar feeding involves similarities in shape, such as ant mimicry mode to that of small, modern, nematocerous by spiders in Baltic Amber (Wunderlich, 2000). dipterans, such as biting midges (Grimaldi et al., ! 2005b; Grimaldi and Johnston, 2014). The Special microhabitats elongate, proboscate mouthparts in some forms There are a variety of ephemeral and spatially appear to be siphonate for feeding on a liquid restricted habitats captured by resin flows that are surface, most likely plant secretions (Ren et al., represented in the amber fossil record. For amber- 2009), whereas others had stylate proboscises able producing environments, the most noticeable to pierce skin and imbibe blood (Boucot and microhabitats are: bark and wood; macrofungal Poinar, 2010; Grimaldi and Johnson, 2014). In fruiting bodies, dung, and carrion; phytotelmata; New Jersey Amber, of early late Cretaceous age and resin substrates. Each of these communities is (~88 Ma), there is evidence for pollinating composed of a recurring spectrum of dipterans, including dance flies and hilarimorphid taxonomically similar species, and is trophically flies (Hilarimorphidae) (Grimaldi et al., 2000b), organized into well-contained food webs. These that possibly made the switch from gymnosperm microhabitats are captured by resin flows ranging to angiosperm pollination. from open woodland to closed-canopy forests The Cenozoic spectrum of pollinating insects where resin-producing trees occur and often are becomes more modern-looking by Baltic Amber recognizable contributors to amber biotas. times (~34–37 Ma). For bees, pollinators consist Bark and wood.—The most important and of more recognizable electroapid bees (Fig. 5L), well-documented microhabitat is bark and wood an early offshoot of modern bees. Baltic Amber (Penney, 2002), denizens of which form a has produced several other major bee lineages: significant part of all major deposits, such as extinct Paleomelittidae, and extant Megachilidae Dominican Amber (Henwood, 1993a; Bright and (leafcutting bees), Melittidae (melittid bees), Poinar, 1994; Grimaldi, 1996), Baltic Amber Halictidae (sweat bees), and within the Apidae, (Schedl, 1947; Larsson, 1978) and mid- the pollen-basket possessing (corbiculate) Apinae Cretaceous amber from Archingeay-Les Nouilles (honey bees, bumble bees, orchid bees, and in France (Girard et al., 2009; see also Alonso et stingless bees), and the acorbiculate Nomadiinae al., 2000). This distinctive community consists of (cuckoo bees) and Xylocopinae (carpenter bees) lichens; epiphytic plants; fungi, especially (Engel, 2001). Both corbiculate and acorbiculate ascomycetes; phthiracarid and other oribatid
185 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 mites; a diverse spectrum of wood-associated microhabitat in regions where tree resin is insects, especially heartwood borers, bark copiously produced are organisms that inhabit the engraver, and sap flow beetles; and cambium semi-viscous to hardened resin surfaces. Resin miners dominated by beetle taxa but also sawfly substrates can be considered as a community of borers (Hymenoptera), pith-fleck cambium miners organisms that support a trophic web of (Diptera), and cossid and clearwing moths microorganisms, plants, fungi, and an assortment (Lepidoptera). An associated predator guild of decomposer, fungivore, herbivore, and consists mostly of arachnids. predatory invertebrates, principally arthropods Macrofungal fruiting bodies, dung, and (Henwood, 1993a). Sap and resin flows attract carrion.—Another specialized microhabitat insects (Langenheim, 1990), notably bark and engulfed by resin flows consists of macrofungal ambrosia beetles (Henwood, 1993a), but also fruiting bodies—large, often massive, sporocarps provide an indirect food resource and access to of polypore (bracket) fungi and large mushroom- nest-construction material for a variety of like structures (Poinar, 2001; Poinar and Brown, organisms. Modern resin deposits on bark 2003; Poinar and Buckley, 2007). These large surfaces house distinctive microorganisms (Cotter fungal reproductive and vegetative structures have and Blanchard, 1982), resinicolous fungi a distinctive fauna dominated by small beetles of (Campbell, 1985), sap-flow beetles, resin- various trophic levels, such as rove beetles collecting leafcutter and stingless bees (Johnson, (Staphylinidae), round fungus beetles (Leiodidae), 1983; Gonzalez and Griswold, 2011), their sap flow beetles (Nitidulidae), minute tree-fungus predatory apiomerine assassin bugs (Usinger, beetles (Ciidae), and hairy fungus beetles 1958), and other trophically connected organisms (Mycetophagidae) (Larsson, 1978; Poinar and (Henwood, 1993a). Portions of this biota, often Poinar, 1999). By contrast, dung and carrion with indications of the particular interaction microhabitats, while also engulfed by resin flows, present, have been recovered from Cenozoic have a poorer amber record than either bark and amber, including resinicolous fungi (Rikkinen and wood or macrofungal bodies. Dung and carrion Poinar, 2000; Beimforde and Schmidt, 2011; microhabitats have some taxa in common, mostly Tuovila et al., 2013), apiomerine assassin bugs flies, and include termites (several families), (Poinar, 2010a), stingless bees (Poinar, 1998), and earth-boring dung beetles (Geotrupidae), scarab leafcutter resin-collecting bees (Poinar, 1992b). beetles (Scarabaeidae), dung flies This biota apparently occupied a special (Scatophagidae), scuttle flies (Phoridae), blow microhabitat distinct from the broader wood- and flies (Calliphoridae), and flesh flies bark associated biota. (Sarcophagidae) (Weitschat and Wichard, 2002; ! Martínez-Delclòs et al., 2004). Intraspecific processes and interactions Phytotelmata.—Phytotelmata consist of The fossil amber record documents every ephemeral aquatic microhabitats such as epiphytic major biological activity conducted by terrestrial filmy fern axils, bromeliad tank epiphytes, lianine organisms. A variety of imaging techniques have pitcher plants, and tree holes that typically occur been used to record this biological activity, on bark fissures, exposed root cavities, or on presented in greater detail below. At the trunk-branch crotches. A distinctive biota is subcellular level, reproduction by binary fission contained within the water reservoirs of these has been documented in an amoeba from plants, and includes particular groups of Cenomanian amber from southern Germany damselflies (Odonata), anopheline mosquitoes (Poinar et al., 1993a). From mid-Cretaceous and midge species (Diptera), marsh beetles Spanish amber, a morphological series of fungal (Scirtiidae), water scavenger beetles, predaceous hyphae display the formation of intercellular diving beetles, and small vertebrates such as clamp connections (Ascaso et al., 2005; Speranza lizards and tree frogs (Poinar, 2010b). et al., 2010). At a more macroscopic scale is an The special microhabitats discussed above— example of frozen behavior from Dominican macrofungi, dung, carrion and phytotelmata— Amber, which documents a lek of termites caught occasionally are captured by resin flows, in a nuptial flight preparatory to mating (Fig. 6C). providing a unique taphonomic window into A pair of long-legged flies, also from Dominican biotic communities and food webs that otherwise Amber, is prepositioned for immediate copulation would be a very rare part of the fossil record. (Fig. 6K); and a pair of moth flies is shown in Resin substrates.― O n e n e g l e c t e d copulo (Fig. 6J). A common pollinator from
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Dominican Amber, the fossil bee Proplebeia from dense tropical rainforest to cool-temperate dominicana, is preserved providing resin and conifer forest (Langenheim, 1990), and, when pollen to conspecific larval nestmates (Fig. 6L; these biomes intersect shorelines of oceans, Poinar 1992a). marine organisms, typically protists and small ! invertebrates, can be entombed in amber (Fig. 4P– BIASES OF THE AMBER FOSSIL RECORD R; Girard et al., 2009). ! The principal bias in virtually all amber Several studies have investigated the differential deposits is organism size. Underrepresented representation of taxa in amber as compared to organisms are those larger than ~1 cm, which are that of equivalent modern biotas, and concluded rarely incorporated in amber. Small, highly that there are important biases in the amber fossil mobile vertebrates such as geckos and tree frogs record: overrepresentation, underrepresentation, frequently are found incomplete (Fig. 6M), likely and no bias. In practice, an assessment of bias can the consequence of predation of partially exposed be tricky because the amber deposit must be tissue. Large arthropods such as scorpions, sufficiently comparable in taxonomic diversity, centipedes, dragonflies, katydids, scarab beetles, s p e c i m e n a b u n d a n c e , a n d e c o l o g i c a l and digger wasps similarly are rarely encountered representation to an analogous present-day in amber, attributable to an ability to free environment such that valid comparisons can be themselves from resin entrapment (Poinar, 1999a; made. In addition, a comparison of biotas from Weitschat and Wichard, 2002). ecologically analogous extinct and modern biotas S i z e i s n o t t h e o n l y r e a s o n f o r presumes that collector bias, either reflected in a underrepresentation of organisms in amber. One fossil deposit or in a recent analog, is not a factor. factor is sedentary versus highly mobile life Given these constraints, the two most relevant habits. For Dominican Amber spiders, wandering deposits for understanding bias in the amber fossil taxa are more prone to inclusion in resin than record are Dominican and Baltic ambers (Penney sedentary taxa (Penney, 2002). An affiliation with and Langan, 2005). The Dominican Amber particular microhabitats, such as wood and bark, deposit is more relevant because the macrofungal fruiting bodies, dung, carrion, environmental conditions under which the biota phytotelmata, and resin substrates are relevant as was deposited were very similar to that of well. Of these microhabitats, organisms inhabiting Hispaniola today (Penney, 2005b), with an wood and bark, macrofungal fruiting bodies, and emphasis on riparian habitats of lower elevation resin substrates are preferentially enriched in (Henwood, 1993b). By contrast, older Baltic amber (Larsson, 1978; Poinar, 1994; Weitschat Amber has its closest taxonomic parallel with and Wichard, 2002) over those organisms southeast Asian biotas, and thus is more occurring in dung, carrion, and phytotelmata. spatiotemporally removed than that of Dominican Insects that swarm and form leks immediately Amber. after emergence as adults occur, albeit Amber deposits only sample terrestrial occasionally, as massive conglomerations within biomes that have amber-producing trees and amber (Poinar, 1992a). Highly fluidized resins shrubs. Consequently, regions such as deserts, often capture large numbers of winged termites in grasslands, steppe, taiga, and tundra lack nuptial flights (Fig. 6C); certain mayfly and representation in the amber fossil record. Within nematocerous fly taxa also swarm in lek those forested and woodland biomes sampled by formations, often close to the ground, and amber, several particular habitats are not present eventually can become entombed in high numbers in the amber record, such as glacially associated as well (Weitschat and Wichard, 2002). Also, it habitats, and non-woody vegetation associated would appear that pest-outbreak taxa should with large lakes (recognizing that amber occasionally be overrepresented (Labandeira, originating and possessing inclusions from nearby 2012), but outbreak frequencies would have to be resiniferous habitats frequently occur in lake sufficiently common to be captured in resin. The deposits). With these caveats aside, and with the reason for the high abundance of ants in certain exception of highly xeric and hydric biomes, the Cenozoic ambers (Grimaldi, 1996; LaPolla et al., general pattern is that amber potentially captures 2013) is difficult to discern. Elevated ant nearly all of Earth’s terrestrial surface that has abundance may be attributable to their very high been colonized by trees and shrubs. Biomes intrinsic abundance and speciosity; or, because documented by the amber fossil record range they are mostly social insects and tend to travel in
187 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 very abundant, monospecific columns; or, as flotation of bulk sediments (McAlpine and active predators of virtually all terrestrial Martin, 1969; Pike, 1993; Corral et al., 1999); invertebrates and vertebrates, they are large quarrying operations, such as excavations overrepresented at flowing resin sites where from open-pit mines, dredging of river deposits partially engulfed prey items were exposed for and mechanized massive shoveling with a consumption (Hölldobler and Wilson, 1990; backhoe (Corral et al., 1999; Weitschat and Grimaldi, 1996; LaPolla et al., 2013). By contrast, Wichard, 2002, 2010); or more limited collections winged insects involved in herbivory and directly from outcrops (Corral et al., 1999; pollination that occur more than a few meters Perkovsky, 2010). Collection of amber from above ground level are poorly represented in outcrops typically involves lignite-rich strata amber (Larsson, 1978). Insects occurring at (Grimaldi et al., 2000a), either exposed on the ground level and in the uppermost soil, regardless surface (McAlpine and Martin, 1969; Hand et al., of their feeding habits, are overrepresented in 2010), or in underground tunnels (Penney, 2010a). amber. Raw amber, which is visually unimpressive, The way amber is collected in the field or requires further processing in which the pieces are archived in collections frequently induces an sorted, then some are cut with a rock saw anthropogenic bias. Any field collecting equipped with a thin, synthetic diamond blade to procedure or archival sorting strategy that eliminate excess material that would impede differentially selects for amber clasts by size, viewing of the inner inclusions. Subsequent shape, appearance, preservational state, preparation involves washing in an ultrasonic taxonomic composition of inclusions, or some cleaner, followed by grinding and polishing the other quality introduces a bias, particularly if pieces into very rounded specimens resembling there are few specimens per clast. One way to the size and shape of gravel (Penney and Green, overcome such biases is to include clasts in 2010). Sufficient optical distance between the collections that contain as many organism edge of the inclusion and the amber outer surface inclusions as possible, such that each clast should be allowed, such that the entombed samples a greater number of available amber organism is not exposed to the external specimens and species within the biota. environment, especially degradative oxidation of ! tissues from contact with air. APPROACHES TOWARD THE STUDY ! OF AMBER Amber conservation ! Especially in geologically older ambers, Each amber clast takes a long journey from the embedding is required to rejuvenate individual field to representation in a publication. In this specimens for viewing (Nascimbene and section, the steps by which amber is processed for Silverstein, 2000). Embedding of amber includes microphotography and analyses are discussed. specimens that are too small and difficult to The various types of light, epifluorescence, handle, such as angular chips, and larger pieces scanning-electron and transmission-electron that have deep fissures and a patchwork of surface microscopy for production of high-resolution cracks (crazing), or specimens that are otherwise images are detailed. More recent techniques that too weathered and brittle and thus are unstable employ microtomographic methods that (Fig. 7A). Embedding requires immersion and nondestructively assemble composite images into suspension of individual amber pieces in a three-dimensional renderings, and analytic synthetic resin or Canada balsam of the same techniques that assess the composition of amber hardness and refractive index as the amber (Fig. matrix and its biotic inclusions, such as various 7B; Santiago-Blay, pers. comm., 2011). The types of spectrometry, chromatography, X-ray amber is placed in cube- or rectangular-shaped microtomography and time-of-flight secondary plastic molds, the walls of which are composed of ion mass spectrometry (Sutton, 2008) also are a plastic that should not chemically react with the discussed. synthetic resin. Typical embedding media are the ! resins Epotek® 301 (Peñalver and Delclòs, 2010) Preparation and documentation and Buehler Epoxicure® (Schmidt, et al., 2012). Historically, amber has been collected in the The molds are filled to three-fourths capacity with field by a variety of techniques. These methods synthetic polyester resin and hardener (Fig. 7C), include: disaggregation, sieving, and saltwater placed in a vacuum chamber, and then
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FIGURE 7.—Steps in the transformation of raw, unprocessed amber of probable dipterocarpacean origin into a high-value collection. This material is Arkansas Amber, from lower middle Eocene strata, central Arkansas Coastal Plain near Malvern, Arkansas (Saunders et al., 1974). A) Unprocessed amber chips and angular to rounded clasts ranging in size from ~2 mm to ~2 cm long. B) Two clasts of washed amber. C) Workstation including a vacuum pump (left), vacuum chamber (center) and polishing wheel (right). D) Amber that has been embedded but not extracted from their plastic containers. E) Amber pieces from (D) at left that have been sawn, trimmed, polished, and surface-coated with nail hardener. F) The finished archival collection. immediately followed by immersion of the amber imperfections or occluding micro-particles. This pieces such that they are suspended in synthetic should be done in a dust-free environment if resin without touching the mold walls (Corral, possible. The amber blocks then are placed in 1999; Hoffeins, 2001). Each of the transparent appropriately sized archival trays with paper plastic molds can hold a single, large piece or identification and provenance data (Fig. 7F). This several, smaller pieces of amber (Fig. 7D). Care general process is used for the conservation of should be taken that bubbles are eliminated, amber, and is particularly important for older particularly at the amber‒resin interface (Corral, ambers, such as those of Cretaceous and 1999; Penney and Green 2010). After the plastic Paleogene age. Older ambers often are fragile, container-resin-amber block has hardened (Fig. highly fractured, and have discolored, denatured 7E), a circular diamond saw with a very thin rinds that have undergone crazing, oxidation, diamond blade can be used to saw off extraneous surface discoloration, a general increase in thicknesses of the sides of the block, followed by opacity, and other chemically degradative the standard amber techniques of grinding and processes (Williams, 1990; Bisulca et al. 2012). polishing. The use of paper archival materials is urged for Each side of the solid amber-containing block permanence of the collection, such as middle is coated with a lacquer, such as clear fingernail Eocene Arkansas Amber (Saunders et al., 1974) in polish, that hardens and smooths any surface the Department of Paleobiology at the National
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Museum of Natural History (Fig. 7). At this point, avoided, as the amber surface may be destroyed s p e c i m e n s a r e r e a d y f o r m i c r o - a n d (Schönborn et al., 1999; Schmidt et al., 2012). macrophotography (Crichton and Carrió, 2007). The specimen then can be viewed under high One modification of the amber-embedding magnification with transmitted light microscopy technique involves fixing cover slips onto the two (Girard et al., 2009). Standard high-resolution exposed surfaces of a thinly sawed and polished light microscopy allows nondestructive amber wafer (Perrichot, 2005). Alternatively, a observation of amber whether organisms are small specimen can be emplaced on a microscope situated partly exposed in fissures or completely slide with a hemispheroidal well, followed by entombed (Beimforde and Schmidt, 2011; flooding the specimen with Canada balsam, and Ragazzi and Schmidt, 2011). Otherwise, viewing placement of a cover slip on the upper surface of preferably is done under two other techniques— the slide for viewing (Penney and Green, 2010). bright-field and/or differential interference An alternative technique avoids the embedding microscopy. Bright-field microscopy consists of a process altogether and dissolves out biological illuminating a sample by white light, typically inclusions from the amber matrix using a solvent under a compound microscope (Fig. 2I-J). In such as chloroform (Azar, 1997; Penney et al., differential interference microscopy, also known 2013b). However, this technique is destructive as Nomarski microscopy, a polarized light source and risks major loss of biological information. fitted with condensers and variable polarizing ! filters is used to improve contrast and clarity of Imaging, processing, and analyses observed specimens. Both bright-field and Light microscopy.—Light microscopy is the differential interference microscopy have been standard, traditional method for examining used extensively in amber studies (Schmidt et al., inclusions in amber. Amber pieces require 2004; Girard et al., 2008) and often are the default significant processing to allow ideal viewing viewing modes when other methods are conditions under a stereo- or compound unavailable. microscope. For stereomicroscope observation, Recent improvement in image clarity, and the each piece needs to be manipulated in three- addition of three-dimensionality to specimens, dimensional space below the focal plane such that have benefited by various techniques such as the best image can be generated from a tiling. Tiling consists of computer-assisted combination of incident light from above and software that uses input from microscope images illumination from the sides and bottom. to achieve a three-dimensional rendering of two- Embedding may be used to stabilize the amber dimensional images. Tiling involves stitching pieces and improve clarity of the amber for together multiple images in the generation of a viewing by eliminating surface boundaries of single, composite, two-dimensional image within different refractive indices associated with deeper a focal plane. Tiling also requires stacking, or the fissures, pits, and surface crazing. Various viscous integration of a vertical series of successive focal- oils of appropriate refractive index, such as an plane images, for rendering into a single, adjusted paraffin oil-alkylaromate mixture composite, three-dimensional image. The (Schmidt et al., 2004), have been used, but this production of a three-dimensionally rendered also degrades the amber, so caution must be image from a series of two-dimensional exercised. The most common and preferred microscope images allows greater clarity, detail, embedding medium is Canada balsam (Girard et and understanding of biological microstructure al., 2009). Various optical immersion oils have (Schmidt et al., 2010). been used (Girard et al., 2011), but they Epifluorescence microscopy.—Epifluor- irreversibly change the optical qualities of escence microscopy is a method of viewing small surrounding amber. specimens using a high-energy light source that Alternatively, visual observation can be made emits a broad, intense spectrum of light ranging by mounting a thin slice of amber with inclusion from visible through ultraviolet wavelengths. material and adding distilled or, preferably, sugar- Most epifluorescence microscopes use incident saturated water, which evaporates much less illumination above the specimen from a light quickly, on a microscope coverslip placed over source that collects and condenses light into a the amber slice. Optical oil can slowly dissolve beam, typically a bright blue color. A desired the amber, and its use is not suggested. Contact wavelength of light appropriate to the specimen is between the amber and oil medium should be the excitation level, which is selected by three sets
190 LABANDEIRA: AMBER of filters (termed the fluorescent cube), One TEM-based study examined cross-sections of responsible for filtering and varying the light dance fly flight muscle in comparison to the same wavelength. Particular organic molecules, such as tissue types from modern, equivalent tissue from melanin pigments, spider chitin, and even the a blow fly (Fig. 2B–C; Henwood, 1992b). In a materials in ambient lint, absorb epifluorescent separate study (Grimaldi et al., 1994), flight light, the re-radiation of which creates the effect muscle tissue, connective tissue attached to flight of fluorescence. muscle, and brain tissue of the stingless bee Several studies have published results from Proplebeia dominicana, also from Dominican epifluorescence of amber inclusions. In a study of Amber, were examined under TEM and deemed a Baltic Amber cypress twig with preserved comparable in preservation to that of modern tissues, Koller et al. (2005) showed strong insect taxa. Similarly, a TEM study of a sectioned, fluorescence of cuticle and resin canals within stained juniper leaf revealed all major foliar internal foliar tissues. Another example from the tissues were well preserved, including cuticle, Álava Amber of Spain, fluorescence occurred epidermis, parenchyma, and phloem and xylem of within protist (Ascaso et al., 2005) and fungal vascular tissue, as well as the specialized (Speranza et al., 2010) microorganisms. Other structures of resin canals, tracheid-like cells, and studies of epifluorescence indicate that pollen stomatal pores (Koller et al., 2005). A very high strongly fluoresces (Ren et al., 2009), suggesting level of specimen preservation is required to applicability to amber material. effectively delineate histological, cellular and Transmission electron microscopy.—Trans- subcellular structure under TEM. mission electron microscopy (TEM) is a Confocal laser-scanning microscopy.—Con- technique that is used mostly for tissues and other focal laser-scanning microscopy (CLSM) is a biomedical materials that are ultrathin, are microscope-based method for generating focused relatively translucent, and can be seen under a optical images of specimens at selected depths. microscope with transmitted light. For TEM, an This process, termed serial optical sectioning, image results when electrons are transmitted uses a scanning laser beam that produces an through the specimen, wherein areas of greater or electronic image similar to a scanning electron lesser density provide the contrast in intensity, micrograph. This procedure allows for imaging translated into grayscale hues. This image is along one focal plane at a time, with subtractions projected or focused onto a fluorescent screen and of the original laser beam not emanating at the often recorded through a camera as a digital focal plane, to achieve complete visualization of image. Based on the physics involving the very an object’s inner structure. These images then are narrow wavelength of electrons, TEM can imported into a computer-based three-dimensional produce images thousands of times more highly or four-dimensional rendering program (in the magnified than any light microscope. Whereas case of a CLSM with time-lapse capability). This higher-magnification images typically reveal procedure involves the stacking and stitching accurate structures in a sample, the varied together of serial images for a highly focused, interactions of waves in TEM can introduce three-dimensional rendered image. In the case of artifacts that require further scrutiny by a skilled amber and other non-opaque objects where TEM operator for correct interpretation of images. illumination can reveal density boundaries, other The problem of artificial generation of spurious CLSM procedures can be applied. One variation structures also afflicts scanning electron is fluorescence emission, whereby objects at focal microscopy (SEM). microscope planes emit a quality of light that In a limited number of instances, TEM has otherwise would not produce an observable been used successfully for imaging very thin to image, similar to that of epifluorescence ultrathin slices of amber. Unfortunately, such microscopy. slices are thinner than the bodies of most For applications involving amber materials, entombed amber specimens, making TEM of CLSM has been used mostly for microorganisms amber a destructive procedure. However, for in European Cretaceous ambers. Spanish amber microorganisms such as protists, bacteria, fungal from Álava in particular was examined by CLSM spores, and pollen, TEM is a viable method of techniques, revealing amoeba-like, paramecium- analysis. Alternatively, TEM has been used to like, and other protists that contained subcellular examine the ultrastructure of tissues within amber structures such as pseudopodia, anterior and inclusions, particularly from Dominican Amber. recurrent flagellae, oral grooves, and vacuoles
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(Ascaso et al., 2003). The vacuoles were which produce data that can be used for assessing preserved as ‘molds’ seemingly adpressed against the relative distribution of atomic elements based the cell walls (Ascaso et al., 2003, 2005). From on their atomic number. By contrast, cathode the same deposit, septate and aseptate hyphae that luminescence (CL) involves a detector that displayed germinal bud development, perhaps captures excited, high-energy electrons as light. preliminary to spore development, were found, as Energy-dispersive X-ray spectroscopy (EDS) is a well as the encompassing cellular membranes and special technique that is applicable to modern and internal organellar structures of algae (Ascaso et fossil resins, and will be discussed later. al., 2003, 2005; Speranza et al., 2010) were Examination of essentially mummified tissues found. Filamentous structures reminiscent of within inclusions is one of the practical uses of bacteria also were preserved (Ascaso et al., 2003). SEM that has documented the high preservation CLSM is a powerful technique for examining potential of amber (De Palma et al., 2010). In an microorganisms and their organellar and cell-wall extensive study (Grimaldi et al., 1994), the tissues substructure, but requires exceptional, pristine of five Dominican Amber insects and a Hymenaea preservation to be useful in examining amber protera leaflet were scrutinized. In the same inclusions. study, two indeterminate long-legged flies and Scanning electron microscopy.—Scanning two fungus gnats were examined. Tissues from all electron microscopy (SEM) has had a major internal regions of the insect’s bodies were distinguished history of an exploratory technique scanned, revealing highly detailed structure of the for documenting microscopic to ultramicroscopic bee’s glossate mouthparts, protocerebral portion structures in scientific and industrial research. of the brain, head, sucking pump, esophagus, SEM operates by producing a directed electron thoracic musculature, and clumps of pollen on the beam from an electron gun that discharges a high- body exoskeletal surface (Grimaldi et al., 1994). energy electron beam onto a surface-clean Under higher resolution and magnification, specimen. This discharge occurs under an micromorphological detail was revealed for a elevated vacuum at the bottom of a vertical scuttle fly, including antennal sensillae and brain cylindrical chamber to produce a focused image. tissue. Mycangial cavities with fungal spores, The image is achieved by the electron beam ventricular (Fig. 2H–I) and pyloric portions of the scanning across the surface of the examined intestinal tract, and malpighian tubules were specimen, which interacts with surface atoms. The examined in an ambrosia beetle (Grimaldi et al., impact of the electron beam produces a variety of 1994). The internal foliar structure of the H. secondary subatomic forms of energy, including protera leaflet also was exposed (Fig. 2G). Using secondary electrons, backscattered electrons, SEM, Henwood (1992b) examined the internal cathode-luminescent light, x-rays, anatomy of an undetermined sap-flow beetle and electromagnetic current, and the original a soldier beetle, showing the complex structure of transmitted electrons. A detector then captures the proventricular valve within the intestinal tract secondary forms of energy as electrons or other (Fig. 2A), as well as the structure of the types of particulate- or wave-based energy that compound eyes and thoracic respiratory and originate from the sample surface. The emission muscle structures. In a more targeted study spectrum detector is attached to an interface that (Briggs and Kear, 1993), SEM images were includes imaging controls and processing produced of muscle sarcolemma, fibrils, and the Z software that provides a black-and-white image of and M fibrillar bands of the recent shrimp the specimen on a video monitor. The images are Palaemon, resembling the results of Grimaldi et produced at a wide variety of magnifications that al. (1994) in many details. reveal detail from ~1 nm to a few mm in length One particular use of SEM for study of amber that, at low magnifications, overlaps with light inclusions is in the backscattered electron mode microscopy. (SEM-BSE), which provides images of specimens Although there are several types of emitted that employ contrast based on the atomic number electrons and other types of radiation, typically of the target. In one study of lower Cretaceous SEMs have a signal detector that retrieves only Álava Amber from Spain (Martín-Gonzales et al., one type of radiation. The most widely used and 2008), the inner organellar structure of the protists standard type of detector captures secondary Euglena, Phacus, Chlamydomonas, and others electrons. One special application of SEM is a were examined. The authors concluded that there detector that images backscattered electrons, was evolutionary stasis from 100 Ma to the
192 LABANDEIRA: AMBER present. In a parallel study (Martínez-Gonzalez et occurring in the pyrenoid body, high Fe at the al., 2009), SEM-BSE provided evidence for how chloroplast cell wall and in general cytoplasm, amber-entombed protists were and the rest of the cell exhibiting enriched Al, K, penecontemporaneously pyritized, a process the and Fe. authors called ‘double fossilization.’ Pyrolysis gas chromatography-mass Energy dispersive X-ray spectroscopy.— spectrometry.—Pyrolysis gas chromatography- Energy-dispersive X-ray spectroscopy (EDS) is a mass spectrometry (Py-GC-MS) is a type of technique for element analysis, such as the spatial chemical analysis that uses a sample heated to the distribution of elements on a sample of interest point of molecular decomposition in order to within a SEM vacuum chamber. EDS provides a characterize the resulting production of smaller frequency-distribution spectrum of elements biomolecules. In Py-GC-MS the thermal based on their characteristic excitation states for destructuring of materials, or pyrolysis, occurs in each of their distinct atomic nuclei. Distinctive a vacuum where a variety of heating techniques excitation states for each atomic nucleus are are used, although commonly the sample contacts determined by the specific amount of energy, a conducting element such as a platinum filament, measured in the amount of kilo-electron volts and is heated to 600‒1000°C. The molecular (KeV) required for electrons of a particular fragments that have been thermally cleaved are unknown isotope at an unexcited ground state to then analyzed by standard gas chromatography be ejected at an excited state to the superjacent techniques; the segregated molecular fragments electron shell bound to the atom’s nucleus. The are indicated by a gas chromatogram output. resulting electron ‘hole’ is replaced by an electron Because of the variety of degraded molecular from the subjacent shell. The difference in energy species produced from pyrolysis, gas between the subjacent lower-energy shell and the chromatograms are difficult to interpret. superjacent higher-energy shell is released as an Nevertheless, with experience in technique, X-ray. The amount of this emitted energy, knowledge of fossil material with complex together with knowledge of the atomic structure organic signatures such as amber, specific of the relevant atomic nucleus, provides for ‘fingerprints’ can be developed and recognized for identification, measurement of abundance, and bulk identification of chemically stereotyped spatial distribution of the emitting element. Often, varieties of amber. The use of Py-GC-MS the accuracy of chemical determinations varies, typically involves qualitative identification, and can be compromised by different elements particularly the polymeric resins that constitute registering the same or undifferentiable peaks. In (to greater or less degree) all ambers. In summary, such cases, the detector fails to capture all of the Py-GC-MS is generally poor for producing useful individual X-rays emitted by the sample atomic quantitative data. nuclei, resulting in poor segregation of the An interesting application of Py-GC-MS for characteristic signatures of each element. understanding amber chemistry is determining the Analyses of amber by EDS in several studies provenance of ambers whose botanical source have resulted in determination of the amber remains contentious. Romanian Amber, of early (matrix) composition surrounding the inclusions. Oligocene age and known as ‘rumanite,’ was In one study of a Baltic Amber leafhopper considered very similar to Baltic Amber and (Kowalewska and Szwedo, 2009), EDS analyses thought to share the same botanical source (Stout of distinctive amber matrices surrounding insect et al., 2000). Examinations of the botanical carcasses pieced together the sequence of short- affinity of Romanian Amber after its discovery in term events leading to the initial onset of the 1930s suggested a confusing array of potential amberization, or diagenesis, within the amber. sources, including cupressaceous, pinaceous (both These transformations included early reducing Abies and Pinus), and an angiosperm origin in the conditions and pyrite formation. In another study Fabaceae. From an extensive analysis of 13 involving Spanish Álava Amber, quantitative EDS representative samples of Romanian Amber, it analyses demonstrated that mineralization of was concluded that the botanical source was, fungal hyphae under anoxic conditions probably indeed, the same as Baltic Amber, but there were occurred soon before amberization (Speranza et subtle compositional differences attributable to al., 2010). For a third use of EDS data (Ascaso et varying degrees of elevated thermal maturation al., 2005), fossil microalgae were found to be (Stout, 2000). differentially mineralized, with elevated Si A similar analysis of latest early Cretaceous
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Álava Amber using gas chromatography indicated solids, such as anisotropic amber with molecules an araucarian origin (Alonso et al., 2000). A later, not in motion, can be accomplished by the variant more robust study using chemical fingerprinting technique of solid-state nuclear magnetic techniques of Py-GC-MS supported an araucarian resonance spectroscopy. One limitation of solid- origin as well, but with an interesting state NMR spectroscopy is the dependence on development in that the identification was done sample orientation to visualization of the on the chemically transformed compounds and molecular structure, requiring multiple iterations not the original primary resin terpenoids, as is the of sample position to achieve better molecular case with much younger Baltic Amber (Chaler characterization. A second hindrance is the and Grimalt, 2005). In late Triassic Dolomites lessening of isotopic nuclear magnetic Amber, Py-GC-MS analyses identified amber interactions when the sample is spun, a samples to a Class II resin (Lambert et al., 2008), consequence that can be remediated by certain indicating that the source plant was a member of corrective actions. the Cheirolepidiaceae, consistent with associated There have been few applications of NMR botanical context of the deposit (Roghi et al., spectroscopy to the examination of amber 2006) composition in the fossil record. Most of the Nuclear magnetic resonance spectroscopy.— application of NMR spectroscopy has been Nuclear magnetic resonance spectroscopy (NMR devoted to general characterization of modern spectroscopy) is an exploratory and confirmatory exudates, such as resins, gums, kinos, and latexes technique for determining the chemical and (Lambert et al., 2008). More specific applications physical properties of atoms within objects by involve examination of the evolution of exudate taking advantage of the magnetic properties in types within major clades of the Fabaceae certain atomic nuclei. Detailed data on the (Lambert et al., 2009). One example from the structure, electromagnetic state, and chemical earliest amber record is the physiochemical context of molecules are provided by characterization of late Triassic Dolomites amber, characterization of their nuclear magnetic using NMR spectroscopy (Roghi et al., 2006). resonance and changes in their resonance From a 13C-NMR-spectroscopy analysis, the frequency. NMR spectroscopy uses atomic nuclei results indicated a complex pattern of thermal that are placed in an electromagnetic field and maturation for the Triassic amber, consistent with r e c o r d s t h e f r e q u e n c y a b s o r p t i o n o f Py-GC-MS analyses. electromagnetic radiation that is distinctive for X-ray computed tomography.—X-ray each particular isotope. This resonant frequency computed tomography (X-ray CT) is a procedure of absorption is proportional to the isotope’s by which two-dimensional virtual tomographic magnetic field, and involves the difference in slices are produced by digital geometric energy between the two spin states—one in processing of a scanned object without the conformity to the magnetic field and the other in laborious process of actual physical sectioning. opposition. Through a complicated process of This procedure allows a viewer to assessing each local, unique energy-absorption nondestructively ‘penetrate’ into an object to frequency of a particular molecule species relative obtain a three-dimensional rendering of an inner to the reference frequency resulting from the structure from a series of integrated, radiographic, externally applied magnetic field strength, a two-dimensional slices about an axis of rotation. distinctive ‘chemical shift’ is produced for each X-ray CT allows three-dimensional renderings to molecular species. This chemical shift provides be manipulated remotely by computer, such as data on the structure of molecular species, usually object rotation along preselected axes of rotation, at levels of ppm. or to traverse across a series of slices to examine Any sample that possesses atomic nuclei with the virtual appearance and disappearance of electromagnetic spin can be characterized by objects of interest, or for a closer inspection of NMR spectroscopy, although the most appropriate microstructure. X-ray CT results are effective samples tend to be organic molecules, including because the incident X-ray beams take advantage those that occur in plant exudates such as gums of density differences along interfaces of the and resins. These samples can be examined using examined object, allowing accentuation of three-or four-dimensional techniques, usually in surfaces. A synonym for X-ray CT is computed relatively large quantities of 2‒50 mg, preferably axial tomography (CAT scan), often used for dissolved in a solvent. However, analyses of medical applications. Special applications of X-
194 LABANDEIRA: AMBER ray CT are positron emission tomography (PET) possible by very-high-resolution X-ray CT of the and single-photon emission computed male pedipalpal surface (Penney et al., 2007). A tomography (SPECT), defined principally by different structure required for systematic differences in the energy source. assignment was provided by a Baltic Amber Beginning in the early 2000s (e.g., Polcyn et specimen of a big-headed fly (Pipunculidae) (Fig. al., 2002), X-ray CT offered an entirely new mode 8J), in which details of the male genitalia, in for visualizing the amber fossil record with the particular the phallic guide complex and related benefits of a nondestructive technique. Although gonopods (Fig. 8K), allowed placement of the almost all of the samples examined were from the specimen into a new species of an extant genus Cenozoic, this technique was extended to (Kehlmaier et al., 2014). A similar basis for Mesozoic ambers (De Palma et al., 2010); by assignment was available for a new Baltic Amber contrast, X-ray CT also was used to characterize strepsipteran genus, Eocenoxenos, whose inclusions in very recent copal and resin. In one antennae was examined using X-ray CT (Fig. 8I), study, Bosselaers et al. (2010), described a a result of which was a considerably earlier time- modern liocranid spider, and compared it to a of-origin of the related strepsipteran lineage conspecific specimen from few-hundred-year-old Corioxenidae (Henderickx et al., 2013). Last, a Madagascaran copal—a comparison made minuscule Baltic Amber astigmatid mite was possible by X-ray CT imaging of the male found attached, apparently in-situ, to the dorsal pedipalp, without which a species-level carapace of a dysderid spider (Dunlop et al., determination would not have been possible. In 2012). The imaging of the 176-µm long phoretic Neogene Dominican Amber, an example of mite (Fig. 8A) indicates the limits of X-ray CT springtail phoresis on a mayfly was established resolution, although X-ray synchrotron (Fig. 8D–E), documenting a unique paired microtomography, discussed next, can render association for the first time either in the fossil or even smaller specimens. modern record of this group (Penney et al., X-ray synchrotron microtomography.— 2012a). Also imaged from Dominican Amber was Synchrotron radiation-based computed an anole skull (Fig. 8L), whose species-group microtomography (SRµCT) is a technique that membership indicated establishment of a broader examines a volumetric structure and renders clade of Caribbean anoles on Hispaniola volume within objects by the two-dimensional sometime during the mid-Oligocene (Polcyn et projection of volumes (Tafforeau et al., 2006). al., 2002). The volume is produced by a scanner along Amber from older deposits, such as Baltic and increments of microns-thick slices within a fixed similar ambers represent the greatest application volumetric grid. With an ultrafine spatial of X-ray CT analyses. Some legacy Baltic Amber resolution on a micron scale, SRµCT can measure collections are historically old, dating to more the attenuation via varying electromagnetic fields than 160 years since first collected, and have of accelerator-produced high-energy electrons in deteriorated as the amber has oxidized, resulting three-dimensional samples. This attenuation in specimens correspondingly being difficult to results in emission of powerful electromagnetic recognize. X-ray CT has rescued some of these waves, termed synchrotron radiation. Synchrotron specimens by imaging: for example, a huntsman radiation can allow for quantitative measurement spider from the Berendt Collection in Berlin was that is not compromised by X-ray beam hardening assigned to a modern pantropical genus of the examined material. One variant of SRµCT representing a major time and range extension for is phase-contrast imaging, in which the difference the family (Dunlop et al, 2011). Another between the refractive index of an object of specimen, a pseudoscorpion, had an opaque outer interest and its surroundings can cause a phase- surface because of a layer of milky, clouded shift, or interference pattern. The resulting amber covering almost the entire body (Fig. 8B). interference pattern augments contrast, and often The specimen was rendered visible by X-ray CT reveals exquisite three-dimensional detail. (Fig. 8C), allowing confident attribution of the SRµCT has had a dramatic impact on imaging species to an extant genus (Henderickx et al., of inclusions in amber, particularly for 2006), an assignment that otherwise would have manipulation of insects to reveal minute been impossible. An additional species ultrastructural detail. Although not supplanting X- assignment was made for a minute spider of early ray CT, SRµCT has supplemented the earlier Eocene amber from the Paris Basin, made technique of X-ray CT by penetrating specimen
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196 LABANDEIRA: AMBER microstructure at even higher levels of paleogeography of its larger, encompassing clade magnification. However, access at a synchrotron (Edgecombe et al., 2012). Another study facility may be limited, and only a few major (Heethoff et al., 2009) explored the degree to facilities are available in scheduling beam time which resolution of very fine-grained for specimen microimaging, such as Argonne micromorphological detail can be resolved for an (U.S.A.) and Grenoble (France). The advantages oribatid mite only 1200 µm long, including of SRµCT, other than revealing extraordinary minute cuticular sculpturing. In an examination of micromorphological detail, include more efficient a Baltic Amber leiodid beetle (Fig. 8G), and using penetration of visually opaque amber specimens a phase-contrast modification of SRµCT, Perreau than X-ray CT, and, in conjunction with X-ray and Tafforeau (2011) explored a virtual, three- fluorescence, the production of elemental maps, dimensional dissection of brain tissue (Fig. 8H), including trace-element mapping, revealing the and the three-dimensional rendering of internal presence of molecules such as melanin and external male genitalic structure. (McNamara, 2013), analogous to EDS analyses. There has been an emphasis on the Although used in compression-impression examination of Cretaceous European ambers deposits for three-dimensional rendering (e.g., using SRµCT. One exception was the anatomy of seeds) (Smith et al., 2009), Cenozoic ambers the Baltic Amber strepsipteran Mengea tertiaria show heightened practical possibilities for SRµCT that was analyzed, including impressive imaging (Soriano et al., 2010). In a study of the taxonomic of the internal organs, allowing placement of this placement of a Chiapas Amber centipede, the specimen within the Strepsiptera, the twisted- micromorphological detail of the character-rich wing parasites (Pohl et al., 2010). In another study head and forcipules (poison organ) allowed a of a moth fly (Psychodidae) from Cenomanian clearer establishment of the phylogeny and past Amber of France (Lak et al., 2008b), the
← FIGURE 8.—Examples of X-ray computed tomography (X-ray CT) and X-ray synchrotron microtomography (SRµCT) techniques for three-dimensional imaging of amber. A) X-ray CT visualization of a minuscule phoretic mite deuteronymph (white arrow) on the dorsal carapace of a middle Eocene Baltic amber dysderid spider at top in (1), with scale bar indicated; (2-5) are various rotational views of the mite, including a collective scale bar and an enlarged image of the attached mite in (6); ms=movable suckers; p1=apodemes; st=sternum; sucker plate=sp; third pair of legs=le3; from Dunlop et al., 2012; fig. 1, specimen SMNG-07/36290. B) Pseudoscorpion Pseudogarypus pangaea, from Baltic Amber shown under visible light microscopy; note near-complete obscuring of opisthosomal dorsal detail (Henderickx et al., 2006; fig. 1, specimen MRAC-219415). C) The same specimen as (B) shown as a visualization under X-ray CT; note detail of opisthosomal segments. D) X-ray CT of early Miocene mayfly Borinquena parva from Dominican amber displaying a miniscule phoretic collembolan (springtail) at the base of the right forewing (Penney et al., 2012a; fig. 1D; specimen PRC-DRA-Eph-002). E) A 4x enlargement of the right forewing and attached phoretic collembolan in (D) above (Penney et al., 2012, fig. 1E). F) Phase contrast SRµCT of the head, mouthparts, and wings of Electrohemiphlebia barucheli from Early Cretaceous (Albian) French amber, validating the appearance of the Hemiphlebiidae during the Jurassic (Lak et al., 2009; fig. 3; ARC-372.1). G). Phase contrast SRµCT of a middle Eocene Baltic amber rove beetle Nemadus microtomographicus, the source of microtomographic dissection in (H) at right (Perreau and Tafforeau, 2011; fig. 1c; specimen BB-1445-K). H) Transverse section of the head in (G) showing the transparency effect of microtomography for the internal expression of the epistomal suture (lower arrow), and brain structure (upper arrow). I). X-ray computed microtomography of the middle Eocene Baltic amber twisted-wing parasitoid Eocenoxenos palintropos, in ventral view revealing distinctive antennomere features that place this taxon as basal member of the Corioxenidae (Henderickx et al., 2013; fig. 2; specimen IG.32.287). J) X-ray computed microtomography in right-lateral view of the Baltic amber big-headed fly, Metanephrocerus hoffeinsorum, in which details in the male genitalia of a related species allowed identification of several congeneric species (Kehlmaier et al., 2014; fig. 11; specimen DB1537-4). K) X-ray computed microtomography of the ventral male abdomen of a related species, M. groehni, showing sternites (e.g., st3), and the genital capsule (arrow) that display the crucial structures of cerci, epandria, and phallic guide complex for species assignment (Kehlmaier et al., 2014; fig. 28; specimen DB1895). L) X-ray computed tomography of a skull of an early Miocene Dominican amber anole lizard, Anolis sp., showing a morphology indicating extreme deep-time longevity of this species complex (Polcyn et al., 2002; fig. 7: SMU-74976). Scale bars: solid=1 mm; dotted=0.1 mm; diagonally lined=1 µm; vertically lined=10 µm; horizontally lined=100 µm. (A, F) Permission for use granted by Wiley-Blackwell. Permission for reproduction of figures 1c and 2a in Perreau and Tafforeau (2011), herein as G and H, is granted by Blackwell Publishing. (J) Permission for reproduction kindly granted by the Palaeontological Association. (L) Permission for use granted by the Society of Vertebrate Paleontology.
197 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 rendering of the external body surface and female compounds. Organic compounds such as those genitalia allowed a better temporally constrained present in amber are essentially destroyed under hypothesis for the origin of the larger subsuming the dynamic mode. However, under the static clade. In a different study. Lak et al. (2009) mode, and when connected to a system that documented phoretic behavior between a compares a molecule suspected to occur in the hitchhiking collembolan (Fig. 8E) and its mayfly sample with a provided standard containing the host (Fig. 8D). Although reporting fossil same or similar molecules, ToF-SIMS can interspecies mutualisms rarely involve computer- reassemble fossilized molecular fragments into based microtome and imaging techniques, one the complete molecule from which they study of Spanish Álava Amber (Peñalver et al., originated. These reconstructed molecules can be 2012) provided intricate detail of a pollinator identified and interpreted by an organic interaction. In this mutualism, two species of the geochemist. One example of the uses of ToF- merothripid Gymnopollisthrips (Thysanoptera) SIMS in compression material was detection of bore specialized pollen-attracting structures that hemoglobin in the abdomen of a middle Eocene included ring setae with affixed clumps of mosquito, using a swine blood standard Cycadopites pollen, preserved in amber within (Greenwalt et al., 2013). strata that contain its likely pollinated seed-plant, ToF-SIMS is the most recent analytical the ginkgoalean Nehvizdyella. method for determining the chemical composition Time of flight‒secondary ion mass of ambers. ToF-SIMS is a powerful technique, spectrometry.—Time-of-flight-secondary ion mass particularly when provided a chemical standard spectrometry (ToF-SIMS) consists of a pulsed ion for calibration in assembling chemical beam shot from a particle-emitting gun within a compounds, and when coupled with computer- vertical chamber, at the bottom of which is a interfacing software for identifying and secured sample of interest. When the ion beam assembling organic molecular structures. One of contacts the outermost surface of the sample, the first examinations of amber composition using molecules are removed (the secondary ions), and ToF-SIMS (Sodhi et al., 2013) was are propelled into the vertical chamber, or flight characterization of Paleogene Baltic and tube, that records the molecular emission from the Bitterfeld ambers, which were compared to sample. The masses of these molecules are previous determinations from techniques such as recorded by a particle detector that measures the gas chromatography. ToF-SIMS analysis exact time for each molecule to reach the detector, confirmed the organic molecular constituents of known as ‘time of flight.’ The exact time of flight, particular ambers elucidated in earlier analyses, measured in nanoseconds, is directly proportional and additionally detected slight differences across to the molecular masses of the compounds that samples. These subtle distinctions, made by ToF- are spalled off the sample impact site. ToF-SIMS SIMS determination of variation in amber operates under several regimes, including surface composition, highlighted the differences in the spectroscopy surface imaging and profiling at provenance, taphonomic history, and age of the depth. Detection of negatively or positively two ambers. Importantly, it indicated that Baltic charged inorganic or organic ions and molecular and Bitterfeld ambers were, indeed, distinct compounds is highly discrete, and molecular deposits and not geographic versions of each masses can be exact, in the range of 1 to 105 other (Sodhi et al., 2013), contrary to earlier atomic mass units, with trace-level detection predictions. In a similar study by Sodhi et al. levels in the range of parts per million. The (2014), twelve diterpenoid resin standards were capabilities of ToF-SIMS include producing provided to ToF-SIMS, which was tasked to output of instantaneous or retrospective spectra of differentiate among larger set of fossil resins with frequency-molecular mass data. known chemical compositions. In that study, ToF- For detection of organic molecules, such as SIMS successfully differentiated the resin polymerized resins in amber, the ToF-SIMS static compositions, with few complications. mode is used, which employs a lower ion beam ! current that teases out ions, molecules, and DISCUSSION: ROLE OF AMBER IN molecular aggregates for special qualitative UNDERSTANDING THE FOSSIL RECORD analyses, as compared to the dynamic mode, ! which uses much more beam current to produce The exceptional taphonomic window provided by data for semiquantitative analyses of organic amber deposits allows a discussion of four themes
198 LABANDEIRA: AMBER that provide a better understanding of the of DNA in resins is common, and lack of terrestrial fossil record. These are: 1) the reproducibility of the resulting data (Penney et al., biomolecular characterization of amber-entombed 2013a). While this episode involving the organisms; 2) phylogenetic reconstruction of idiosyncrasies of amber preservation was o r g a n i s m s f o u n d i n a m b e r ; 3 ) t h e disappointing to some, these events do point to macroevolutionary patterns of amber taxa; and 4) the taphonomic limitations of amber. The degrees paleobiogeographic inferences resulting from the of amber preservation are based on the biological distribution of amber taxa. For each theme, there level of organization: what is preserved at the are particularly noteworthy examples that organ level may not be preserved at the tissue illustrate the importance of amber in illustrating level; and excellent preservation at the tissue level the fossil history of terrestrial life. does not ensure that constituent cellular and ! organellar levels are preserved; and perhaps most Biomolecular characterization disappointing of all, evidently biomolecules such Amber-entombed tissues of arthropods in as proteins, lipids, carbohydrates, and DNA are Dominican and Baltic ambers display a probably not preserved intact in deep time, at least remarkable state of preservation. Microorganisms older than ~ 1 Ma (Rogers et al., 2000; Hebsgaard from older, mid-Cretaceous ambers of Spain and et al., 2005). Nevertheless, there are heartening France similarly exhibit exceptional retention of signs that, in limited instances, sufficient, original subcellular organellar detail. Because of this molecular structure is retained for subsequent exceptional preservation, it was once thought that reassembly of molecular fragments with ToF- the retention of biological structure could extend SIMS technology, or other techniques (Allentoft to lower levels of biological organization to et al., 2009). Evidently, 44-million-year-old include not only cells and organelles, but also degraded hemoglobin fragments can be biomolecules such as proteins and DNA. At about reconstructed into a viable biomolecule the same time that histological microstructure was (Greenwalt et al., 2013), and carotenoid pigment being fleshed out (e.g., Henwood, 1992a, b), there structure can be retrieved from preserved feathers were published studies that claimed that DNA in younger Dominican Amber (Thomas et al., isolated from amber organisms was sequenced 2014). and characterized (Poinar, 1994). Specifically, the ! claim was DNA was sequenced from a Phylogenetic reconstruction nemonychid weevil Libanorhinus succineus from Several examples have been presented where Lebanese Amber (Cano et al., 1993), and two d e t a i l e d r e s o l u t i o n o f i m p o r t a n t species from Dominican Amber, the termite micromorphological structures, particularly Mastotermes electrodominicanus (DeSalle et al., involving genitalic characters, were crucial for 1992, 1993) and the bee Proplebeia dominicana taxonomic assignment to a modern clade (e.g., (Cano et al., 1992). In addition, the Dominican Polcyn et al., 2002; Penney et al., 2007; Amber resin-producing source plant, Hymenaea Henderickx et al., 2013; Kehlmaier et al., 2014). protera, presumably also had characterizable These revised assignments almost always had DNA (Poinar et al., 1993c, 1994). A bacterium three effects. First was resolution of species comparable to modern Bacillus sphaericus, was phylogenetic relationships within the large clade revived and cultured, and sequenced, after containing the fossils. Second was downward presumably surviving a ~17 Ma interval in a piece temporal extension of the modern clade of Dominican Amber (Cano and Borucki, 1995; containing the newly described fossil, indicating also see Yousten and Rippere, 1997; Greenblatt et an earlier time of origin. Third was the extension al., 2004). of the broader encompassing clade that includes In 1997 and 1998, several studies could not the fossil and sister clades to an even earlier time confirm the results of DNA sequences retrieved of origin, often to the Mesozoic for many from multimillion-year-old amber insects (Austin Cenozoic forms. The overall effect of preservation et al., 1997a, b; Smith and Austin, 1997; Walden of exquisite micromorphological detail in amber and Robertson, 1997; Gutiérrez and Marín, 1998). is to more adequately resolve systematic These follow-up reports detected a variety of relationships among taxa. This produces a more issues in the original studies, including error-free tree of life, at least for those organisms insufficient internal laboratory checks of results, that entered the taphonomic window of an other studies indicating that extensive degradation exceptional amber deposit.
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Macroevolutionary patterns modern clades, many of which consist of There are three patterns that the amber fossil herbivores that interacted with gymnosperms record contributes to understanding the broader (Labandeira, 2014). Included among these earlier sweep of macroevolutionary processes. The first insect lineages are the Protopsyllidiidae, involves mid-Mesozoic protists that presumably Burmacoccidae, Albicocociidae and show an amazing amount of evolutionary stasis, Schizopteridae (all Hemiptera), Caloblattinidae assuming that any potential organellar, (Blattodea), Elcanidae (Orthoptera), integumentary or other intracellular differences Lophioneuridae (Thysanoptera), Nemonychidae are recognizable. Examples of microorganismic a n d B e l i d a e ( C o l e o p t e r a ) , stasis was indicated for ~110 Ma mid-Cretaceous Pseudopolycentropodidae and Mesopsychidae Spanish amber (Martín-Gonzalez et al., 2008; ( M e c o p t e r a ) , a n d S e r p h i t i d a e a n d Peñalver and Delclòs, 2010), that affected a Stigmaphronidae (Hymenoptera) (Kuschel and variety of protistan taxa at the generic level. Poinar, 1993; Grimaldi et al, 2002, 2005b; However, as in the studies of disease transmission Grimaldi, 2003; Grimaldi and Ross, 2004; Koteja, in Myanmar amber, the presence of evolutionary 2004; Nel et al., 2007; Ren et al., 2009; Peñalver stasis has not been convincing, and some of the and Grimaldi, 2010; Ortega-Blanco et al., 2011a, structures described may be artifacts (Girard et b; Labandeira, 2010, 2014). Overlapping with al., 2011). A more compelling case are several these older plant and insect lineages in these studies demonstrating evolutionary stasis in deposits are modern ‘paleoherb’ grade and other protists from mid-Cretaceous (Cenomanian) early lineages of angiosperms, centered in the late Schiersee Amber of the southern Alps, slightly Cretaceous and Paleogene, many of which were younger than the age of Spanish Amber, although interacting with insect lineages that became erroneously reported earlier to be of Triassic age dominant during the late Cretaceous and (Schmidt et al., 2001). Schiersee Amber Cenozoic. More derived, modern lineages of microorganisms include cyanobacteria, amoebae, insects occurring in these same deposits include protists, and fungal spores (Poinar et al., 1993a, b; the Tettigoniidae and Tetigridae (katydids and Schönborn et al., 1999; Schmidt et al., 2004, pigmy grasshoppers, Orthoptera), Thripidae 2006). While mid-Cretaceous German and (common thrips, Thysanoptera), Curculionidae Spanish ambers display considerable evolutionary and Chrysomelidae (common weevils and leaf stasis for microorganisms, the co-occurring beetles, Coleoptera), Melittosphecidae, arthropods provide evidence for evolutionary Formicidae and the Scolebythidae (the earliest turnover. One interesting study of a considerably bee, the earliest ants, and scolebythid wasps, more recent example of stasis involves a Hymenoptera), the Cecidomyiidae, Empididae, spirochete symbiont in the termite Mastotermes and Therevidae (gall midges, dance flies, and electrodominicus from Dominican Amber (Wier stiletto flies, Diptera), and the Gracillariidae (leaf- et al., 2002). blotch miner moths, Lepidoptera) (Kuschel and The second pattern documents changes in the Poinar, 1993; Labandeira et al, 1994; Poinar and composition of insect faunas during the early to Danforth, 2006; LaPolla et al., 2013; Labandeira, mid-Cretaceous. An intriguing aspect of amber 2010, 2014). deposits during this time interval involves insect These three amber deposits sample the last taxa occurring in principally Lebanese Amber occurrences of insects that either became extinct (Azar et al., 2010), Álava Amber (Peñalver and or underwent substantially reduced diversities Delclòs, 2010) and Myanmar Amber (Ross et al., from a greater presence in a formerly 2010), collectively ranging from ~120‒100 Ma. gymnosperm-dominated world. At the same time, These deposits capture a mix of species that the three amber deposits also record the earliest represent the two major evolutionary biotas of the appearing insect lineages that became dominant in terrestrial Mesozoic. Represented from earlier the more recent, angiosperm-dominated world. biotas are gymnosperm lineages (which peaked in Although never rigorously studied, perhaps the Jurassic), such as cycads, cheirolepidiaceous because of inadequate sample size at the family or and araucariaceous conifers, corystosperms, genus levels, three outcomes of this transitional bennettitaleans, and a range of ginkgophytes, interval of time would have been elevated often as pollen or smaller foliage elements. These extinction rates, elevated origination rates, and an deposits also contain many extinct or currently overall decrease in insect diversity during the shift relict insect lineages phylogenetically basal to from gymnosperm- to angiosperm-dominated
200 LABANDEIRA: AMBER biotas (Labandeira and Sepkoski, 1993; differences in an insular versus a continental Labandeira, 2014). setting, or that the age of Baltic Amber is about A third pattern is attributable to the twice that of Dominican Amber, thus allowing preservation of evidence for disease transmission, greater time for biogeographical divergence; or evident especially in Dominican, Baltic, and perhaps the effects of Pliocene‒Pleistocene Myanmar ambers (Table 2,
201 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 20 organism in micromorphological detail. grassland, desert, tundra, taiga, steppe, glacial, Nevertheless, some compression-impression and aquatic habitats such as lakes. Although deposits are almost as well-preserved as amber amber sometimes is deposited in lacustrine or deposits, such as the late Miocene Calico shallow-marine nearshore environments, the Mountains hot-spring deposit of southern source material almost always originated from California (Palmer, 1957; Park and Downing, wooded or forested habitats. 2001) and the middle Eocene Kishenehn biota ! from western Montana (Greenwalt and ACKNOWLEDGMENTS Labandeira 2013; Greenwalt et al., 2013). ! Trophic data.—The amber fossil record Thanks go to Finnegan Marsh for rendering preserves splendid inter-organismic trophic data. Figures 2-8. I am grateful to Xavier Delclòs of the These data could best be put to use by an University of Barcelona for granting permission exhaustive study of the trophic relationships of to reproduce Figure 1. Tom Phillips of the one spatiotemporally constrained abundant and University of Illinois at Urbana-Champaign diverse amber deposit using the food-web provided the acetate-peel image for Figure 3A. techniques used for the Messel food web (Dunne Figure 4A is courtesy of Stefano Castelli of the et al., 2014; Labandeira and Dunne, 2014). University of Padova; Figure 4B, courtesy of Parasites, pathogens, and disease.—The Guido Roghi of the University of Padova, Italy; amber fossil record is very good for documenting and Figures 4D‒G courtesy of Alexander Schmidt parasite, pathogen, and disease relationships of the University of Göttingen, Germany. Enrique among animals (Poinar, 2014). The compression- Peñalver of the Institute of Geology and Mines in impression fossil record is much better, by Madrid, Spain, provided images for Figures 4J–N. contrast, for recording plant diseases, including I am also grateful for Patrick Craig for supplying their pathogens, vectors, and hosts (Labandeira images for Figures 5 and 6. This contribution and Prevec, 2014) benefitted significantly form discussions with ! Jorge Santiago-Blay and two anonymous Advantages of compression-impression reviewers. This is contribution 298 of the deposits Evolution of Terrestrial Ecosystems consortium at Greater temporal completeness.—The the National Museum of Natural History, in compression-impression record of megascopic Washington, D.C. fossils is more complete, and replaces, with minor ! exceptions, the amber fossil record from the REFERENCES Paleozoic to mid-early Cretaceous, before the ! onset of Lebanese Amber (Labandeira, 1999). The AGEE, H. R., AND R. S. PATTERSON. 1983. Spectral mid-Cretaceous fossil record does have rare sensitivity of stable, face, and horn flies and flies biological inclusions, but they are and behavioral responses of stable flies to visual overwhelmingly microorganisms (Schmidt et al. traps (Diptera: Muscidae). Environmental 2006) or very rare arthropods (Schmidt et al., Entomology, 12:1823‒1828. 2012). ALENCAR, J. C. 1982. Estudos silviculturais de uma população natural de Copaifera multijuga Hayne An expanse of two-dimensional surfaces.— —Leguminosae, na Amazonia Central. 2. The compression-impression fossil record allows Produção de óleoresina. Acta Amazonica, 12:75‒ for two-dimensional examination and analysis of 89. herbivory (Wilf and Labandeira, 1999; ALIMOHAMMADIAN, H., A. SAHNI, R. PUTNAIK, R. S. Labandeira et al., 2007), which requires fossils in RANA, AND H. SINGH. 2005. First record of an layered beds that display an extensive amount of exceptionally diverse and well-preserved amber- foliar surface area. The type of research involving embedded biota from Lower Eocene (~52 Ma) quantification plant-insect interactional data is not lignites, Vastan, Gujarat. Current Science, 89: possible by examining amber material. 1328‒1330. Range of environments.—The compression- ALLENTOFT, M. E., S. C. SCHLEUSTER, R. N. impression record samples a broader range of HOLDAWAY, M. L. HALE, E. MCLAY, C. OSKAM, M. T. P. GILBERT, P. SPENCER, E. WILLERSLEV, environments, some of which are essentially AND M. BUNCE. 2009. Identification of absent in the amber fossil record. Environments microsatellites from an ancient moa species using not sampled by the amber fossil record are where high-throughput (454) sequence data. resin-producing trees are absent, and include
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