THE EXCEPTIONAL PRESERVATION OF PLANT FOSSILS: A REVIEW OF TAPHONOMIC PATHWAYS AND BIASES IN THE FOSSIL RECORD

—The exceptional preservation of plant fossils falls into two categories: whole plant preservation and anatomical detail. Whole plant preservation is controlled primarily by transport and event preservation (e.g., ash falls), whereas anatomical preservation can occur through one of several taphonomic pathways: compression-impression, silicification, coal-ball formation, pyritization, and charcoalification. This review focuses on these taphonomic pathways, highlighting important factors and controls on the exceptional preservation of plants. Special emphasis is given to data garnered from experimental and actualistic approaches. INTRODUCTION ! What is exceptional plant preservation? Plants are fundamentally different from animals in several ways, and expectations for ‘exceptional preservation’ must change accordingly. Plants are modular organisms that readily disarticulate into various organs (leaves, stems, roots, and reproductive structures). Unlike animals, disarticulation occurs regularly over a plant’s normal life cycle (e.g., deciduous trees shed leaves every autumn) as well as upon death (Spicer, 1989; Greenwood, 1991; Wing et al., 1992; Rowe and Speck, 1998; Gee and Gastaldo, 2005). The tissues of these organs are somewhat different from those of animals: the structural polysaccharides (cellulose, hemicellulose, and lignin) and waxy polymers comprising the cuticle (Briggs et al., 2000; Briggs, 2003; Fioretto et al., 2005; Wakeham and Canuel, 2006; Gupta et al., 2007a, b) have a much lower preservation potential than bones or shells, but are also much more likely to be preserved than animal soft parts. Most importantly, the way in which these plant parts find their way into the lithosphere is fundamentally different from the pathways followed by terrestrial or marine animals. Many marine invertebrates, like plants, disseminate propagules throughout the water column, but these are almost never preserved. In contrast, plant propagules (seeds, pollen) are exceptionally well preserved in great abundance and diversity throughout much of the Phanerozoic record. Similarly, although both terrestrial vertebrates and plant hard parts (stems, trunks) are preferentially preserved in fluvial deposits or debris flows, there is a strong ecological control on what types of plants grow or accumulate near water bodies (e.g., calamitaleans and sigillarian lycopsids during the Carboniferous and Permian periods; vines in the Cenozoic era), whereas these patterns are sometimes less clear for animal groups. Therefore, at the most basic level, the processes controlling plant fossilization are distinct from those affecting animals. Exceptionally preserved plant fossils fall into two main categories. One type of exceptionally preserved plant fossil retains the entire and original arrangement of the various organs—from roots to reproductive structures (Scott and Rex, 1985). If organs are found separately, they are given distinct names, and only when two structures are found together can the complete plant be reconstructed, as was the case with Archaeopteris (Beck, 1960a, b). Fossils such as these are dependent on transport processes and unusual events such as ash falls (Ferguson, 2005). The second type of exceptional fossil preserves the internal structure and three-dimensional cellular detail. Although uncommon, such preservation can provide paleobotanists with unique taxonomic information (Smoot, 1984; Smoot and Taylor, 1986). This type of preservation is controlled by preand post-burial decay and diagenesis. 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 Why study exceptionally preserved plant fossils? The fossil record of land plants extends into the middle Ordovician. Numerous microfossils— spores, tubules, and cuticle fragments—are reported from Ordovician marine rocks around the world (Gensel 2008). Several authors (e.g., Gray et al., 1985; Wellman et al., 2003) suggested taxonomic placement of at least some of these microfossils within the bryophytes (hornworts, liverworts, and mosses), the sister groups to all other vascular plants (Nickrent et al., 2000; Nishiyama et al., 2004), based on the preserved anatomy, whereas vascular plant fossils do not appear until the late Silurian (Gensel, 2008). The majority of plant fossils are preserved as either impressions (no organics remaining) or compressions (organics remain) (Collinson, 2011); these fossils are part of a continuum of more to less preserved organic material. Surface details, such as stomata, trichome bases, and epidermal cell arrangement may be preserved with or without organic remains, but the preservation of the ultrastructure of internal leaf anatomy varies widely. Woody organs, such as the axes and roots, are more often found preserved in three dimensions, but delicate tissues (e.g., cellulose-rich, lignin-poor phloem) are often not preserved due to more rapid decay. Plant fossils from Lagerstätten can retain this internal anatomy and provide more morphological detail than the average compression-impression fossils. The early Devonian Rhynie Chert Lagerstätte, for example, contains a rich, in-situ assemblage where the anatomy of early plants and other organisms are silicified and preserve exceptional detail. This exceptional fossil deposit is one of several that have helped reveal major changes in plant evolution throughout the Phanerozoic (Table 1; Schopf, 1975; Knoll, 1985; Gensel, 2008). Additionally, the exceptional preservation of both the external morphology and internal anatomy of plants has allowed the study of the evolution of plant vascular systems (e.g., Wilson et al., 2009) and entire plant ecosystems (Scott and Rex, 1985). Without exceptionally preserved fossils and fossil assemblages, these ins igh ts in to the pas t would be los t . Understanding how these fossils form is crucial to the interpretation of the functional and ecological information they hold. This paper will review the major taphonomic pathways leading to the exceptional preservation of plants, with a focus on experimental and actualistic studies of plant preservation. TAPHONOMIC PATHWAYS ! Three major concerns in the formation of plant fossils are: 1) how well anatomically important information is retained; 2) the taxonomic biases that may be introduced during the fossilization p roces s ; and 3 ) t he deg ree t o wh ich paleoenvironmental data (e.g. , isotopic information in cuticle waxes) are retained. The basic pathway for a plant organ, such as a leaf, to become a fossil is for it to be transported, buried, undergo some degree of decay, and survive long enough for the surrounding sediment to lithify (Rex and Chaloner, 1983; Ferguson, 2005), or for the tissues to be permineralized (e.g., Kenrick and Edwards, 1988). The highly resistant waxy cuticle is thought to favor this process (Collinson, 2011) by providing a robust external layer of protection to the more labile internal tissues of the leaf, but the degree of internal decay, as well as exposure to oxygen, will affect the final product (Yang and Huang, 2003). Different taphonomic modes occur on different timescales and under different environmental conditions, and may affect the formation of a fossil at different parts of the pathway to fossilization (Fig. 1). Additionally, tissues and organs may be preserved differently by different taphonomic pathways (Fig. 2). Schopf (1975) presented a classic view on the four preservational modes that are important in fossil plant preservation: 1) duripartic (hard part) preservation, 2) organic compression/impression, 3) authigenic preservation, and 4) cellular permineralization. An addit ional mode, charcoalification, was recognized as an important mode of preservation, particularly of flowers, in the 1980s (e.g., Friis and Skarby, 1981). Paleontologists have long recognized that duripartic preservation is the most common, as evidenced by the extensive marine shelly fossil record. Authigenic mineralization occurs when the surrounding sediment is rapidly cemented, normally in the form of a concretion (Schopf, 1975). McCoy (2014) discusses the formation of concretions, so it is not considered here. Plant fossils are most often preserved as either impressions or compressions (Schopf, 1975; Greenwood, 1991), but often retain only gross morphological characters or epidermal anatomy through the preservation of the durable cuticle. Permineralized fossils can be the most useful to paleobotanists because internal anatomy is often