Introduction To Paleobotany, How Fossil Plants Are Formed

1 INTRODUCTION TO PALEOBOTANY, HOW FOSSIL PLANTS ARE FORMED WHAT IS PALEOBOTANY? .............................................................1

Cellular Preservation ...........................................................................23 Unaltered Plant Material .....................................................................30

THE OBJECTIVES OF PALEOBOTANY ..................................... 2

Summary Discussion ..........................................................................34

Reconstructing the Plants......................................................................2 Evolution of Plant Groups.....................................................................3

PALYNOLOGY ..................................................................................34

Form and Function in Fossil Plants .......................................................4

Geochronology and Biostratigraphy ...................................................36

Biostratigraphy and Correlation............................................................4

Paleoecology .......................................................................................37

Paleoecology: Plants in Their Environment ..........................................5

ABSOLUTE DATING ......................................................................38

Determining Paleoclimate from Fossil Plants .......................................6 GEOLOGIC TIMESCALE ..............................................................39

Summary ...............................................................................................7

BIOLOGICAL CORRELATION .................................................. 40

PRESERVATION: HOW PLANT FOSSILS ARE FORMED AND PRESERVED ............................................... 8

SYSTEMATICS AND CLASSIFICATION ................................ 40

Depositional Environments of Fossil Plants .........................................8

Nomenclature of Fossil Plants ............................................................41

Compressions ......................................................................................10

Classification of Organisms ................................................................42

Coal and Charcoal ...............................................................................18 BACKGROUND READING.........................................................42

Impressions .........................................................................................21 Molds and Casts ..................................................................................22

The Earth is a vast cemetery where the rocks are tombstones on which the buried dead have written their own epitaphs. Louis Agassiz … intoxicated joy and amazement at the beauty and grandeur of this world, of which man can just form a faint notion. Albert Einstein

WHAT IS PALEOBOTANY?

no flowering plants, and when the continental land masses were in different positions than they are today. Who has not been captivated by the various forms of life that are recorded in the rocks and the enormous reconstructions of dinosaurs exhibited in various museums? It is natural to wonder about such examples of prehistoric life—how these organisms

Humans are by nature curious, and we are all interested in the Earth on which we live and how various aspects have changed through geologic time. We speculate about what the Earth looked like when there were no trees, when there were

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paleobotany: the biology and evolution of fossil plants

lived, what their patterns of behavior were, and even why they became extinct. Although the paleontologist is interested in the geologic history of animals, the paleobotanist is concerned with the plants that inhabited the Earth throughout geologic time (Ward, 1885) (FIG. 1.1). In a general sense, the paleobotanist is a plant historian who attempts to piece together the intricate and complicated picture of the history of the plant kingdom. Although molecular and genetic analyses of living plants have become increasingly important as tools in reconstructing the phylogeny and evolutionary history of plants, the discipline of paleobotany, in all its various forms, remains the only method by which this history can be documented and visualized. Two books that discuss paleobotany from a historical perspective and that capture the excitement of the discipline are The Fossil Hunters—In Search of Ancient Plants (Andrews, 1980) and History of Palaeobotany—Selected Essays (Bowden et al., 2005). These volumes discuss the origins of the field and the scientists who have made the science so exciting and fascinating. Fossil plants and floras from one period of geologic time are different in size and shape, level of complexity, and abundance from those of other time periods. The most logical explanation for these differences is that the types of plants changed, or evolved, through geologic time. Unless one believes that there were an almost infinite number of “special creations,” we must assume that new plant forms were derived from preexisting ones by the processes of evolution. By studying the record of fossil plants, it is possible to assess the time at which various

major groups originated, the time each reached its maximum diversity, and, in the case of certain groups, when they became extinct.

THE OBJECTIVES OF PALEOBOTANY One of the aspects of paleobotany, which makes it unusual and interesting, is that it is inherently interdisciplinary and can be approached from either a biological or a more geological perspective—or both together. Each perspective presents a variety of questions that are unique to that discipline. Today more than ever before, the questions being asked by paleobotanists necessitate that both the botanical and geological perspectives be fully understood. To a large degree, the research questions that paleobotanists ask are influenced by whether their training emphasized a biological or a more geological perspective. RECONSTRUCTING THE PLANTS

Paleobotanists who have been trained primarily as biologists are interested in research directions which include all aspects of the organisms themselves. Because the majority of fossil plants are generally preserved in rocks as disarticulated plant parts (FIG. 1.2), that is leaves (FIG. 1.3), stems, pollen, or reproductive structures, a major aim of paleobotany is to reconstruct the whole plant, that is to say, to put the pieces of the puzzle back together. Once this is accomplished,

Figure 1.2 Figure 1.1 Lester Ward. (Courtesy H.N. Andrews.)

Impression of angiosperm leaf from the Dakota Formation (Cretaceous). Bar ⫽ 2 cm.

chapter 1 introduction to paleobotany, how fossil plants are formed

the research can turn to other areas, such as determining the group of living plants, if any, to which the fossil is most closely related. Some paleobotanists are interested in aspects of plant life history that can be determined from fossils. For example, how did these plants reproduce, and how and what types of propagules were disseminated? Are their reproductive strategies similar to those of closely related living plants, or have there been major modifications in the reproductive systems of certain types of plants through geologic time? If so, how did this happen and when? What can we determine about the environment in which the plants lived millions of years ago, based on features of the fossil plants? For example, fossil wood collected from the Permian and Triassic of Antarctica (FIG. 1.4) indicates that the climate was quite

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favorable for tree growth, based on the analysis of tree rings (FIGS. 1.5, 1.6). General circulation models of Permian paleoclimate, however, have proposed that these high paleolatitudes were very cold and not favorable for plant growth. Some paleobotanists are interested in what strategies these plants, and the animals that lived among them, developed to survive in the extreme seasonality at polar latitudes. EVOLUTION OF PLANT GROUPS

Paleobotanists are also interested in the origin and subsequent evolution of major groups of plants and their interrelationships. When did plants first inhabit the Earth and what did they look like? When did the first representatives of different groups of plants first arise? Other researchers want

Figure 1.4

Permineralized wood extending from paleostream channel in the Triassic of Antarctica.

Figure 1.3 Compressed pinna showing detail of pinnule venation (Cretaceous). Bar ⫽ 2 cm.

Figure 1.5

Section of Antarctic wood (Triassic) showing several growth rings. Bar ⫽ 1.4 mm.

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paleobotany: the biology and evolution of fossil plants

Figure 1.6

Frost ring in Triassic permineralized wood from Antarctica. Bar ⫽ 3 mm.

to know why certain types of plants developed the capacity to produce secondary tissues (such as wood), whereas others have remained small throughout their geologic history. A number of paleobotanists study not only the plants themselves, but also the interactions of the plants with other organisms in the environment, especially the symbiotic interrelationships between plants and other organisms. For example, today almost all terrestrial plants possess mutualistic associations with fungi that inhabit their roots (mycorrhizae). Paleobotanists want to know when and why these associations became established, why they are absent in some groups today, and why only certain types of fungi form these associations. Can the fossil record of plants tell us anything about various biological activities that existed millions of years ago, such as the interactions between plants and certain groups of animals that use plants for food or protection? What types of evidence can be used, and what information does this provide about the interdependence of organisms through time? Can we determine from the fossil record if plants possessed certain features that served to attract pollinators, or produced edible seeds, or whether some plants produced certain chemicals that deterred herbivory? The answer to all these questions is a resounding YES! There is a multitude of information that can be gleaned from careful examination of the plant fossil record, and the types of information that we can obtain are constantly increasing as more and more research is done on fossil plants. FORM AND FUNCTION IN FOSSIL PLANTS

From many plant fossils, it is possible to understand the relationship between form and function in ancient plants, that is, what advantages or limitations are imposed on the growth and development of a plant based on certain biomechanical

properties? For example, are all arborescent (treelike) plants constructed of cells and tissue systems of the same type? If not, in what other ways can plants grow to tower over their neighbors? Studies of this type examine the anatomical and morphological properties of various fossil plants, often using computer simulations to model growth, in an attempt to better understand broad evolutionary patterns of plant growth, as well as changes in growth form through time (Niklas, 1992; Rowe and Speck, 1998; Niklas and Spatz, 2004; Niklas et al., 2006). Biomechanical studies have been especially useful in delimiting adaptations necessary for plants to move onto the land, including upright growth, size limitations, and the nature of the conducting strand (Niklas, 1986), and, once plants became established in terrestrial environments, the influences of gravity and wind on their reproduction (Niklas, 1998), and even aerodynamic features of pollen (Schwendemann et al., 2007). Factors such as plant size and form can also be examined over a broad spectrum of plant morphologies and thus offer insights as to why certain plants and plant groups have developed particular anatomical and morphological characteristics. Examining tree growth and other factors in extant plants has demonstrated that there are a variety of variables in play. Because fossils demonstrate a number of different growth forms that are not seen in modern plants, they offer a unique resource of data to allow paleobotanists to explore a host of intriguing biological questions. Fossil plants can also be used to infer developmental processes (Sanders et al., 2007). For example, Boyce and Knoll (2002) analyze the morphospace of numerous Paleozoic leaves representing various clades and show that leaf evolution follows the identical sequence of morphologies in all groups. Such an approach provides the ability to test hypotheses using living leaf development as a proxy for the leaves seen in various groups in the fossil record. BIOSTRATIGRAPHY AND CORRELATION

Paleobotany has also played a key role in many areas of geology, especially in biostratigraphy—placing rock units in stratigraphic order based on the fossils within them. Pollen grains and spores (one aspect of palynology) have been extensively used as index fossils in biostratigraphy and in the correlation of rock units, as have various forms of algal cells and cysts. In some instances, megafossils, such as leaves and seeds, have also provided a method of correlating rock units which are widely separated geographically. Pollen and spores, as well as megafossils, are especially useful in correlating terrestrial rocks, as these are generally deposited in limited areas (former lakes, ponds, river systems, etc.), making correlation by lithology (i.e., rock characteristics) very difficult.

chapter 1 introduction to paleobotany, how fossil plants are formed

1. Lepidophloios 2. Diaphorodendron 3. Synchysidendron 4. Paralycopodites 5. Sigillaria 6. Pteridosperms 7. Tree ferns 8. Sphenopsids

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2

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5

4

A

7 6

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B

Figure 1.7 Transect through a Westphalian D mire showing habitat partitioning among major genera (A) and distribution of other plant

groups (B). (From DiMichele and Phillips, 1994.)

PALEOECOLOGY: PLANTS IN THEIR ENVIRONMENT

Paleoecology, the study of past environments, is a rapidly changing field that involves the integration and synthesis of both botanical and geological information. In recent years there has been a concerted effort by many paleobotanists to understand the paleoenvironment of fossil land plants more completely. For example, Bateman and Scott (1990) examined the famous late Tournaisian (lowermost Carboniferous) plant-bearing deposits at Oxroad Bay, Scotland, from a number of different perspectives, including an analysis of the geologic history and sedimentology of the site, as well as the paleoenvironment and paleoecology of the plants. Their studies indicate that the Oxroad Bay flora is found at eight levels in five successive facies, and these facies show the increasing influence of nearby volcanoes in the ocean-marginal setting. Details of the depositional environments through time at this site make it possible to understand plant adaptations to a rapidly changing, lowland environment, and to better understand both the biological and evolutionary importance of the floras.

Much paleoecological work initially focused on analyses of the swamp vegetation that contributed to extensive coal deposits in the Midcontinent of North America during the Carboniferous (Phillips and Peppers, 1984). The data used in these early analyses came primarily from the study of Pennsylvanian plants in coal balls—nodular concretions of limestone that contain permineralized peat (FIG. 1.5; see section on “Preservation”), coupled with a precise stratigraphic framework for the coal ball deposits based on palynology and careful field observations and measurements. Through the pioneering efforts of Phillips, DiMichele, and coworkers, we now possess an excellent understanding of many aspects of the paleoecology of coal-swamp vegetation during the Carboniferous (Wagner and Diez, 2007). Analysis of the plants preserved at different levels in these deposits not only documents the partitioning of the habitat among the different plant groups along ecological lines (Fig. 1.7), but also records changes in the depositional environment through time (DiMichele and Phillips, 1994; Wagner and Mayoral, 2007). In one study on the peat flora just above the Mahoning coal

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paleobotany: the biology and evolution of fossil plants

in Ohio (Conemaugh Group, Pennsylvanian), DiMichele et al. (1996), utilizing macrofossils, palynomorphs, and coal petrology, concluded that the lepidodendrid trees (lycopsids—see Chapter 9) in this succession were flooded once, recovered, and then finally drowned by another flood event. This type of information can be utilized to recognize regional (Phillips et al., 1985) and global responses of plant communities to climate change (DiMichele et al., 2001a; Wagner and Mayoral, 2007). Understanding the interplay between these swamp-inhabiting plants and a variety of environmental parameters has now made it possible to interpret large-scale ecological shifts (e.g., the role of sea level fluctuations) in the community structure of the swamps, and to examine evolutionary questions within these habitats (DiMichele et al., 1985; DiMichele et al., 1996). These studies in turn have stimulated interdisciplinary research focused on broader questions, for example the evolution of major terrestrial ecosystems through time (Behrensmeyer et al., 1992; DiMichele and Hook, 1992). Paleoecological studies are very important in revealing the diversity of fossil communities inhabiting a geographic area (horizontal variation in floras) at the same time. Wing et al. (1993) examined fossil floras preserved in an ash fall and in fluvial deposits from the Upper Cretaceous (midMaastrichtian) of Wyoming, USA. They found that ferns (49%), along with palmettolike palms (25%), dominated the landscape, and that other angiosperms (Chapter 22), mostly herbaceous dicots, were dominant only in disturbed areas close to streams (fluvial deposits). The flowering plants were more diverse—constituting 61% of the species present—but they represented only 12% of the vegetational cover in this area. This study, and other similar ones (e.g., McElwain et al., 2007), have detailed the difference between the diversity of plants in fossil floras and the dominance of particular taxa within the paleoecosystem. Of course, it is only possible to fully comprehend the fossil assemblages, or taphocoenoses, by comparison with extant plants in various depositional environments (Spicer, 1981; Burnham, 1989, 1997) and by being aware of the taphonomy of fossil plants (Spicer, 1989) (see section on “Preservation”). Understanding and interpreting the sedimentological nature of the fossil assemblage, whether based on megafossils or microfossils, is only one of several aspects required in determining the diversification of plants through geologic time (Wing and DiMichele, 1995; Lupia, 1999). Paleoecologists use many of the same statistical methods used in contemporary ecological studies, including a variety of multivariate methods (Spicer and Hill, 1979; McCune and Grace, 2002). These tools, and many others, now make

it possible to examine the evolutionary and ecological processes that governed the plant communities which we now document as the fossil record (Jackson and Erwin, 2006). For a more in-depth approach to the study and methodologies of plant paleoecology see DiMichele and Wing (1988), Gastaldo (1989), and Jones and Rowe (1999). DETERMINING PALEOCLIMATE FROM FOSSIL PLANTS

Understanding climates of the past has become more and more crucial to appreciating the changes occurring on our warming planet today, and paleobotany is very important in providing baseline data to reconstruct past climates and in calibrating paleoclimate models based on physical parameters (Steppuhn et al., 2007). This area is rapidly expanding, so we will only cover a few of the many ways in which plant fossils can be used to reconstruct paleoclimate: TREE RINGS Data from fossil tree rings (paleodendrology) (FIG. 1.3) represent an important source of paleoclimate information, in some instances with very fine resolution, for example, major atmospheric disturbances (Miller et al., 2006). Although initially used for Holocene climate information (especially dating of archeological sites), some of the techniques used to analyze recent and subfossil wood have been extended to older material (Jefferson, 1982; Creber and Chaloner, 1984a; Creber and Francis, 1999; Taylor and Ryberg, 2007). Based on the changes in radial cell diameter within the tree rings and the variation in ring width (FIG. 1.3), it is possible to extrapolate climate information, which is especially useful when coupled with information from megafossils, microfossils, and the sedimentological record of the site. This approach has been utilized successfully by Parrish and Spicer in their work on Late Cretaceous floras from the North Slope of Alaska (Parrish and Spicer, 1988; Spicer and Parrish, 1990). More recently, Taylor and Ryberg (2007) have examined tree rings in Permian and Triassic woods from Antarctica. Based on their analysis using a variety of techniques, they suggest that the small amount of latewood indicates a very rapid transition to seasonal dormancy in response to decreasing light levels at these high polar latitudes. The mechanisms these plants evolved to cope with life in a polar light regime are of continuing interest in this and other studies based on plants that were once living at very high paleolatitudes. NEAREST LIVING RELATIVE The nearest living relative (NLR) method has been in use since the beginnings of paleobotany, particularly when

chapter 1 introduction to paleobotany, how fossil plants are formed

dealing with late Mesozoic or Cenozoic floras, as these are more likely to have close living relatives. It is based on the premise that climatic tolerances of the fossils are very similar to those of their NLR. The paleobotanist compares as many fossils as possible within a flora to their most closely related extant taxa; the more species in a fossil flora that have NLRs, the more precise the paleoclimate estimate, and the more closely related a fossil taxon is to an extant one, the more precise the method. It depends, therefore, partly on the paleobotanist’s ability to identify the fossils very accurately. The further back in time, the less effective this method is, as more and more extinct species or taxa which have no living relative appear. As a result, NLR has been used to best effect for Cenozoic angiosperm floras (Wolfe, 1995). This method can provide a general estimate of paleoclimate, but is limited by the fact that some fossil taxa do not have the same climatic limitations as their modern counterparts. LEAF PHYSIOGNOMY Leaf physiognomy analysis is a powerful technique that has been widely used in paleobotany to reconstruct Cenozoic paleoclimates. It is based only on angiosperms, however, so its applicability before the Cretaceous is uncertain (but see Glasspool et al., 2004a). Physiognomy is the general appearance of a plant, and it has long been known that plant physiognomy, especially leaf physiognomy, can be related to climate (Bailey and Sinnott, 1916). Physiognomy is primarily independent of taxonomy, for example plants with thick water-storing stems and leaves tend to grow in arid regions of the world, even though they may belong to a number of different families of plants. For fossil floras, this means that leaves do not have to be identified in order to obtain a paleoclimate signal. In his now-classic papers, Jack Wolfe (FIG. 22.276) presented the applications of leaf physiognomy to paleobotany, based on large collections of many leaves from extant floras, which he then was able to compare with Cenozoic angiosperm floras (Wolfe, 1993, 1995). Webb (1959) had previously completed a detailed physiognomic classification of Australian floras, and his definitions of leaf types are generally used in physiognomic methods today. There are presently two methods of leaf physiognomic analysis that are in general use: leaf-area and leaf-margin analysis. Leaf area directly correlates with mean annual precipitation (MAP). CLAMP (Climate-Leaf Analysis Multivariate Program; Wolfe, 1995) measures 31 leaf character states of woody dicots (Chapter 22) and uses multivariate analysis to map leaf shape in two-dimensional space (Wolfe and Spicer, 1999). CLAMP can provide a number of climatic parameters related to precipitation, humidity, and temperature.

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Leaf-margin analysis (LMA) relies on the relationship between leaf margin (toothed versus entire) and climate (Greenwood and Wing, 1995; Wilf, 1997). Specifically, the proportion of leaves in the flora with toothed margins can be correlated with mean annual temperature (MAT), as toothed leaves are more abundant in wet environments. Both CLAMP and LMA can provide quantitative reconstructions of past climates, including estimates of MAT and MAP. More recently, paleobotanists have refined physiognomic methods by using computer image analysis to analyze both leaf-shape and leaf-margin morphology (Huff et al., 2003; Royer et al., 2005). Further data on the ecophysiology of modern plants and the function of various leaf shapes (Royer and Wilf, 2006) will no doubt help to refine these methods and improve their accuracy in the fossil record. Both methods are very robust, as both rely on large databases of leaf physiognomy of living leaves from many different sites and habitats. STOMATAL INDEX The stomatal index (the ratio of the number of stomata to the total number of epidermal cells plus stomata within a given leaf area expressed as percentages; see Salisbury, 1927) has been widely used in recent years to reconstruct past ρCO2 levels, as the stomatal index is inversely proportional to atmospheric CO2 levels. Woodward (1987) was one of the first to demonstrate the value of this relationship for ancient climate prediction, based on comparisons of modern leaves with herbarium specimens from preindustrial times. The best results have been obtained from comparisons of the same genus and species in order to control for genetic differences, so younger fossils, such as Holocene plants, have provided reproducible results (Wagner et al., 2004). The technique has been extended further back in time, for example the Cenozoic (Royer et al., 2001), as well as to the Mesozoic and Paleozoic, although there are limitations to the technique, especially with older fossils (Roth-Nebelsick, 2005; Uhl and Kerp, 2005). For studies in deep time, researchers have coupled CO2 estimates from stomatal indices with other proxy records, such as isotope data (Beerling, 2005 and papers cited therein). A summary of the pros and cons of methods to reconstruct past levels of atmospheric CO2 can be found in Royer (2001) and Kerp (2002). Details regarding the stomatal index technique can be found in Beerling (1999) and Poole and Kürschner (1999). SUMMARY

Throughout this book there are numerous examples of many of the biological and geological questions being asked by

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paleobotany: the biology and evolution of fossil plants

paleobotanists today, and how the fossil record contributes to answering these questions. The field of paleobotany continues to advance, not only by the discovery of new fossils but also by the use of new methods applied to existing fossils and the application of techniques from other fields to paleobotany. Plant parts preserved in different ways or ones that show additional features are continually being discovered. More sophisticated and improved methods to study the fossils and interpret the results also provide new data which contribute to an enhanced understanding of the plants and communities that existed through geologic time.

PRESERVATION: HOW PLANT FOSSILS ARE FORMED AND PRESERVED A relatively small fraction of the plants and other organisms that live on the Earth at any particular time will ever become fossils. Most dead plant material is decayed by aerobic (oxygen-loving) fungi and bacteria. So, the first requirement for fossilization is that dead plants must be deposited in an environment where air is excluded, that is an anaerobic environment. This usually involves deposition in a body of water (discussed below), but not always. Once deposited, the plants must be buried by sediments so that air is excluded. In addition, these sediments must have enough acidity that anaerobic decay is also reduced. Paleobotanists are often asked the question, where do you look for fossil plants? The answer is that they typically are found in places where the rocks containing them have been exposed in some way (FIG. 1.8); these rocks may be as far away as the Arctic (FIG. 1.4) or the Antarctic. Because streams and rivers cut down through the rocks, exposed strata along waterways are often excellent sites to prospect for fossil plants. Erosion by water in many other places also exposes fossil-bearing rocks. Sometimes it is possible to find plants in eroded cliffs along seashores. In addition to the natural exposure of plant-bearing strata, excavations are frequently the source of many fossils. Road cuts, for example, often reveal fresh surfaces with unweathered rocks that contain wellpreserved fossils. As might be expected, quarries and mines are rich sources of fossil plants, revealing rocks that would otherwise have been inaccessible to paleobotanists. Coal balls (FIG. 1.43), a type of permineralization, are frequently encountered in coal mines, and often the shales immediately above the coal seams in such mines contain abundant fossil plants. Quarries in which clay is being excavated for bricks,

Figure 1.8 Students collecting fossil plants from a narrow lens of fine-grained shale.

tiles, or pottery are sites that often provide fossils. In fact, almost any massive construction site, such as for a dam, a hydroelectric plant, or a building with a deep foundation, can, and has, yielded an abundance of fossil plants. DEPOSITIONAL ENVIRONMENTS OF FOSSIL PLANTS

Fossil plants are found in almost all regions of the Earth, the most notable exceptions being recent volcanic islands or in rocks that have been extensively metamorphosed (FIG. 1.9). Marine plants, such as various forms of algae (Chapter 4), are generally found in rocks deposited in marine environments (e.g., nearshore deposits, carbonate shelves, etc.). Although land plants are occasionally found in marine rocks, generally, wherever terrestrial sedimentary rocks occur, there is a good chance that fossil plants will be found in them. Sedimentary rocks are those formed by the accumulation of rock particles derived from the weathering and mechanical abrasion of existing rocks. The great majority of sedimentary rocks are formed by deposition of particles in water, but wind deposits (e.g., eolian sands, loess) can also form, and rock breakdown can occur by chemical weathering, with rock components being released into solution, later to solidify at some other place. Plant parts are typically fossilized, then, in areas where sediment is accumulating. The delta of a river is just such a depositional environment. As the course of the river constantly shifts, channels are abandoned and new ones initiated; natural levees are destroyed during flooding, and new ones built up later. A meandering river cuts into the bank on the outside of each meander, and deposits sediment on the inside of meanders, often covering plants growing along the water. When the river breaks

chapter 1 introduction to paleobotany, how fossil plants are formed

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Figure 1.9 Exposed rocks in Antarctica. Zone of dark red rocks are volcanic and lack fossil plants, including microfossils.

through a levee, a rush of water and sediment, called a splay deposit, can rapidly cover the adjacent floodplain, inundating the plants growing there. Associated with the deltaic system are abandoned stream channels, often referred to as oxbow lakes, and vegetation growing along the banks of these abandoned channels may be undisturbed for some time. If a subsequent flood destroys the levee, knocking down trees and other plants growing on it, these plant parts can be carried to abandoned channels and other places where a high concentration of sediment would bury the plant fragments and fill in the oxbow. As might be expected, plant parts carried for great distances would tend to be fragmented and shredded, and those deposited close to the place of growth would be less distorted and better preserved. Plants that become preserved at the same locality where they were growing are termed autochthonous (e.g., many Pennsylvanian coal ball deposits), whereas those assemblages that have been transported are termed allochthonous. Preservation of whole plants or plant parts (usually stems and roots) in growth position is termed in situ. The plants that once made up a community, together with the other organisms in the ecosystem, are preserved in the Earth’s crust in a variety of ways, and different kinds of physical and chemical processes were involved during the process of preservation (FIG. 1.6). Moreover, various environmental settings and depositional processes also result in fossils that occur in a variety of forms. Taphonomy is the study of all the processes occurring between the time the organism died and its discovery today as a fossil. These include burial by sediments of some type (e.g., sand, fine mud, ash, etc.), and diagenesis, which is defined as all the chemical and physical changes to the sediment (and the fossils within

Figure 1.10 Cuticle preparation of the seed fern Blanzyopteris praedentata showing numerous trichomes extending from the surface. Bar ⫽ 1 mm.

it) as it is converted into rock (Gastaldo, 1989; Gee and Gastaldo, 2005). Because of the countless ways in which plants are preserved, the paleobotanist must employ different techniques to extract the maximum amount of information from fossils. For example, when a paleobotanist finds a fossil leaf, it would first be compared to modern leaves, based simply on the overall size and shape, that is, the morphology of the leaf, to identify it. This can include describing the shape and distribution of teeth on the margin of the leaf, if present, and the shape of the base of the leaf compared to the tip, as well as the length and shape of the petiole. Next, the discoverer might examine the pattern of veins in the leaf—the venation, followed by a microscopic examination of the types and distribution of stomata (pores for gas exchange) and other structures on the surface, such as hairs (trichomes) (FIGS. 1.10, 1.11), or trichome bases if the hairs themselves are no longer attached to the leaf. Still later, the paleobotanist might study the ultrastructure of the cuticle (the waxy

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paleobotany: the biology and evolution of fossil plants

Figure 1.11 Multicellular, uniseriate trichomes on Blanzyopteris praedentata cuticle. Bar ⫽ 400 μm.

covering on leaves), or the molecules that remain part of the leaf after diagenesis (geochemistry). It is possible to determine the proportion of carbon isotopes (13C versus 12C) in many fossil plants, and to use these to reconstruct paleoenvironment or the type of photosynthetic pathway (C3 versus C4 photosynthesis) employed by the plant. And in the future? Perhaps paleobotanists will be able to extract information that reveals details about biochemical pathways, developmental mechanisms, and families of genes involved in response to parasites or herbivores that attacked the leaf surface, all from a fossil plant leaf! Although there are numerous variations on the ways in which plant fossils are preserved, there are a few basic types which we discuss later. It is important to keep in mind, however, that all preservation types can intergrade, or a fossil plant may be preserved in more than one way, for example, a compressed plant with a stem that is partially petrified. Finally, there may be certain structures that appear to be an organism, but are not of organic origin. One of the most common of these are dendrites (FIG. 1.12).

Figure 1.12 Pseudofossil (dendrites) that look like the leaves

of a plant, but are manganese oxide that has grown on the bedding plane of a limestone (Jurassic). Bar ⫽ 2 cm. (Courtesy BSPG.)

COMPRESSIONS

As sediments accumulate, such as in an oxbow lake, water is squeezed out, so the sediments become much more compact, and plant fragments contained within them become flattened (Rex and Chaloner, 1983; Chaloner, 1999a). Internal structure is usually obliterated as the cells become flattened, and frequently all that is left is a delicate carbonaceous film that conforms to the original outline of the plant part. This type of fossil is called a compression (FIG. 1.13), and it is one of the most common types of plant fossils. As you might predict, if the sediment grains that bury the plant parts are large and angular, such as sand grains, the resulting compression

Figure 1.13

Compression specimen of Osmunda claytoniites from the Triassic of Antarctica. Bar ⫽ 2 cm.

shows less detail than if the sediment particles are smooth edged and very fine, such as clay particles (FIG. 1.14). There is a vast range of sediment size and structure; plant parts have even been preserved in conglomerates (rock made up

chapter 1 introduction to paleobotany, how fossil plants are formed

Figure 1.14

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Portion of compressed fern frond (Cretaceous).

Bar ⫽ 2 cm.

of variously sized pebbles), but generally, compressed plants will be better preserved in clays or shales than in sandstone deposits. Compressions are not always formed in deltaic and fluvial (river) systems; they may be formed in lagoons, along meandering rivers (not necessarily near deltas), and in ponds, swamps, or other depositional systems, as well as in wind-blown sediments. Most often a terrestrial ecosystem is involved (as opposed to a marine environment), although there are instances in which terrestrial plants are even preserved in marine limestones. Plant compressions can also be found in consolidated volcanic ash. These fossils represent plants growing near an area where there was volcanic activity that spewed clouds of ash into the air. Often there is severe atmospheric turbulence near a volcano and thunderstorms may develop as a result. The rainwater and the ash make a fine-grained mud which cascades down the hillsides, picking up and burying plant parts as it goes (Burnham and Spicer, 1986). When the mud hardens, it entombs pieces of plant material, in many cases exactly in the position in which they grew (in situ). For example, in the Cretaceous Baqueró Group in Santa Cruz Province,

Figure 1.15 Portion of a fern frond preserved in tuff from Argentina (Cretaceous). Bar ⫽ 2 cm.

southern Patagonia, the tuff deposits were laid down so rapidly that it is possible to trace the fern Gleichenites vertically from the rhizome through the sediments to the leaves (FIG. 1.15) (Archangelsky, 2003). So well preserved are some of the compressions from this site that the plant material can be sectioned and examined with the transmission electron microscope (Archangelsky and Villar de Seoane, 2004). Fossil cytoplasm has even been described in one unusual compression specimen (Hall, 1971) (FIG. 1.16).

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paleobotany: the biology and evolution of fossil plants

Figure 1.17 Compression of pinnae in which only the axes and

pinnule venation are preserved (Pennsylvanian). Bar ⫽ 1 cm.

Figure 1.16

Pollen grain Kollospora extrudens with contents (cytoplasm?) extending from the wall. Bar ⫽ 35 μm. (From Hall, 1971.)

A very unusual kind of matrix in which compressions occasionally occur is diatomite—a rock formed from the siliceous shells (frustules) of diatoms (Bacillariophyceae; see Chapter 4), which today inhabit both fresh water and marine sites. Diatomite is especially fine grained and preservation of plant remains in it is often superb. Since the diatom frustules are actually the cell walls of these microscopic algae, in this method of preservation one organism is serving as the preserving matrix for another organism. Leaves are some of the most common plant parts preserved as compressions (FIG. 1.13) and, in many instances, they occur in numerous, closely spaced layers within the rock matrix. Often a collector can uncover the leaves by splitting the rock along bedding planes with a knife (if the matrix is clay) or with a hammer and chisel (if the rock is harder), although sometimes the paleobotanist must resort to more energetic measures to uncover fossils, such as using a jackhammer or even dynamite! Many compressions are of value in showing surface details and overall morphology. Experimental evidence suggests, however, that the size and shape of fossils can vary depending on the matrix in which they are preserved (Rex, 1986). Such features as leaf shape, presence or absence of

a petiole (leaf stalk), leaf margin, trichomes, and the pattern of venation (FIGS. 1.17, 1.18) are generally readily discernible. In some cases it is possible to examine the distribution of stomata in the leaf surface. When there is an abundance of leaves presumably from one species of plant, it is possible to determine the degree of variability exhibited. In other cases this is far more difficult, especially as leaves tend to be the most plastic in their morphology of any plant part. For example, it is often difficult to find two leaves that are morphologically identical on some modern plants, such as the common mulberry tree (Morus spp.). Many conifers (Chapter 21) produce juvenile leaves with a different morphology than that of mature leaves. When found as fossils, these may have been described as two different species. For these reasons, paleobotanists must be extraordinary sleuths in uncovering features that will help distinguish variability within a single species (intraspecific variability) from differing leaf forms that reflect different species (interspecific variability) or genera. Compressions preserved as relatively dark carbonaceous films on a lighter colored rock matrix make examination and imaging of the fossil relatively easy. Sometimes, however, the matrix and the fossil have similar color values and imaging is more difficult. In these cases, details can be enhanced by using sidelighting (a light source at an oblique angle to the compression) or a polarized light source, or by submerging the fossil in some liquid, such as water, xylene, or alcohol. In many instances, the use of cross-polarization

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Figure 1.19

Arctocarpus cuticle showing paracytic stomata with cuticular ridges (Cretaceous). Bar ⫽ 4 μm. (Courtesy G. R. Upchurch.)

Figure 1.18 Cuticle preparation showing venation of Barthelopteris germari pinnule. Bar ⫽ 1 mm.

(polarized light sources together with a polarizing filter over the camera lens) can significantly enhance contrast (Schaarschmidt, 1973; Crabb, 2001). Another method that has been used with compressed animal remains uses backscattered electron imaging to help differentiate among superimposed anatomical features compressed into a single plane (Orr et al., 2002). CUTICLE Although most compressions show only superficial details, in some instances it is possible to learn a great deal about cellular details of the epidermis from preservation of the cuticle (FIG. 1.19). Primary aerial parts of all vascular land plants are covered with a thin film of waxy material, the cuticle, which prevents excess water loss from the surfaces of the plant. Cuticle is continuous over the surface of the plant, except over the stomatal openings; it is a non-cellular, amorphous layer that is deposited on the outside and into the walls of the epidermal cells. It closely conforms to the contours of the surface of the epidermal

cells and may also extend slightly downward between these cells in flanges which are perpendicular to the surface of the plant. Plant cuticles, as well as waxes deposited on top of the cuticle, are important for the plant in controlling transpiration—the movement of water through the plant, from the roots to its eventual evaporation from the leaves. Most water is lost from stomatal openings, but some can evaporate through the cuticle if it is thin enough or its texture allows for cuticle transpiration. Cuticle is also important in control of gas exchange with the environment, in repelling water from the leaf surface, in attenuation of photosynthetically active radiation (PAR), and in blocking ultraviolet (UV) radiation. The cuticle, especially the leaf cuticle, serves as an interface for a host of biotic interactions between plants and other organisms in their environment, including parasites and herbivores (Riederer and Müller, 2006). Because cuticle is inert and resistant to decay, it is widely preserved in the fossil record, and represents a valuable source of paleobotanical information (Mösle et al., 1997). The leaf cuticle is often preserved as an intact envelope which once surrounded the living leaf tissue (FIG. 1.20). Many fossil cuticles are fragile and must be protected prior to transport from the collecting site. One way to do this is to apply a mixture of nitrocellulose to the surface of the fossil (LePage and Basinger, 1993, 1994), thus preventing loss and breakage of specimens as the freshly excavated sediment dries. Common nail polish has also been used in a similar way. Covering the cuticle with a preservative in the field, however, may prevent subsequent geochemical study of the cuticle (Collinson, 1987).

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paleobotany: the biology and evolution of fossil plants

Figure 1.20 Cuticle preparation of Odontopteris brardii pinnule. Bar ⫽ 1.5 mm.

Figure 1.21 Laboratory set up for preparation of cuticle

Figure 1.22 Pinnule of Pseudomariopteris cordato-ovata showing adaxial epidermal anatomy (Pennsylvanian). Bar ⫽ 1 mm.

mounts from Eocene clay. Note staining jars at left and pieces of cuticle before and after bleaching, right. (Courtesy D. L. Dilcher.)

It is possible to remove the cuticle from many fossil leaf specimens either mechanically, with a needle or brush, or chemically by dissolving away the rock matrix. Pieces of cuticle retrieved in this way can then be bleached and stained with common biological stains, such as safranin (Bartholomew et al., 1970; Dilcher, 1974; Kerp and Krings, 1999; Krings, 2000a) (FIG. 1.21). When mounted on a slide and examined under a microscope, the cuticle or cuticular fragments reveal considerable epidermal detail (Kerp, 1990). Cuticles of epidermal cells are apparent (Fig. 1.22), along

with the structure of the stomatal complex (the cells associated with the pores, i.e., stomata, in the leaf (Fig. 1.23)), the distribution of stomata, presence of hairs or glands, and other distinguishing features. The cuticle in plants is very much like a fingerprint, in that many species have distinctive epidermal features and patterns that can be useful in identification. Furthermore, it is often possible to demonstrate that disarticulated plant parts, such as leaves, stems, flowers, and seeds, actually belong to the same plant because the individual parts have the same complement of cuticle structures.

chapter 1 introduction to paleobotany, how fossil plants are formed

Figure 1.23

Cuticle preparation of Dicksoniites pluckenetii stomatal apparatus. Bar ⫽ 20 μm.

15

Cuticle and epidermal features can be investigated by transferring the compression fossil from the rock matrix in the form of a transparent film, which can then be examined under a microscope. The film can be made by pouring on a liquid-plastic substance (e.g., clear fingernail polish), letting it dry, and then teasing away the film, with the cuticle adhering to it, from the rock matrix. A comparable technique is to embed the surface of the fossil in liquid plastic (such as that used for preparing biological mounts) and then macerating away the rock with an appropriate acid. In some cases, the cuticle can simply be removed from the surface of the rock with a dissecting needle, without the need for transfer film or maceration. Cuticles can also be transferred onto polyester overlays, which reduces the time of preparation and preserves the fossil from which they were taken (Kouwenberg et al., 2006). In addition to preservation of the cuticle (FIG. 1.23), or some chemically altered form of it (see Gupta et al., 2006), some compressions contain cellular remains as part of the carbonaceous layer (Niklas, 1981a). Niklas et al. (1978) embedded and sectioned exquisitely preserved, compressed fossil leaves from the Succor Creek Formation (middle Miocene) of Oregon, USA, for transmission electron microscopy (TEM) and showed that the cellulosic microfibrillar organization of the cell walls could be seen. Even more astounding was the fact that organelles within the mesophyll cells of the leaves, including chloroplasts with grana stacks (FIG. 1.24) and starch deposits, nuclei (FIGS. 1.25,

Figure 1.24 Stacks of grana membranes in the chloroplast of a fossil Betula leaf (Miocene). Bar ⫽ 100 nm. (From Niklas, 1981a.)

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paleobotany: the biology and evolution of fossil plants

Figure 1.25

Lycospora spore with structures interpreted as possible chromosomes (Pennsylvanian) Bar ⫽ 12 μm. Figure 1.26 Tetrad of Flemingites spores showing cell contents interpreted as nuclei (Pennsylvanian). Bar ⫽ 20 μm.

1.26, 10.20) with condensed chromatin, and plasmodesmata, were preserved in these fossils! The possibility always exists, however, that subcellular structures may be contaminants or artifacts formed as a result of the compression and dehydration of other cell components during diagenesis (Niklas, 1982). Chloroplasts have also been reported from Eocene leaves of Metasequoia collected from the Canadian High Arctic (Schoenhut et al., 2004). These authors suggested that the extraordinary preservation may have resulted from high concentrations of tanniniferous cells in the leaves, which may have inhibited microbial degradation and thus left the cell organelles intact. Some compressed Eocene angiosperm leaves from the Geiseltal in Germany and Clarkia beds in Idaho are still green when the rock is split open (FIG. 1.27), which suggests that the chlorophyll is still intact (e.g., Dilcher, 1967). BIOFILMS AND PLANT FOSSIL PRESERVATION The reason that some very delicate structures are preserved is difficult to understand, but in recent years there has been great progress in elucidating the role that various microorganisms, especially those in biofilms, can play in the preservation process (Borkow and Babcock, 2003). Biofilms consist of an aggregation of microorganisms held together in a slimy matrix of extracellular polysaccharides, which are secreted by certain bacteria in the biofilm. We now know that biofilms are ubiquitous on the Earth, and can be found in environments ranging from streams to desert crusts, to hot

Figure 1.27

Compressed angiosperm leaves from the Clarkia beds with chlorophyll preserved (Miocene). Bar ⫽ 3 cm.

springs; the dental plaque on your teeth represents a type of biofilm. One of the first researchers to recognize the importance of biofilms in fossil preservation was Jean-Claude Gall (1990) in his studies of the beautifully preserved, soft-bodied organisms in the Early Triassic Grès à Voltzia Formation (Voltzia Sandstone) in northeastern France. These organisms, both plants and animals, are believed to have been rapidly covered by biofilms which entombed the animals in lowoxygen conditions that inhibited decay. For more information

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TEM of fossil cuticles has proved useful in detailing the intricate structural organization of the stomatal complex in certain fossil plants and in understanding preservation processes (Villar de Seoane, 2003). Fossil cuticles have also been examined for their chemical constituents (Tegelaar et al., 1991; Mösle et al., 2002; Gupta et al., 2006). Some cuticles are too thin for standard preparation techniques to be effective, or have been fragmented into minute pieces during fossilization so that they cannot be removed from the rock surface. Under these circumstances, incident light, dark field, or epifluorescence microscopy have been useful in revealing certain cuticle and epidermal characters (Kerp and Krings, 1999; Thomas et al., 2004). Figure 1.28

Surface of Pseudofrenelopsis cuticle showing distribution of stomata (Cretaceous). Bar ⫽ 15 μm. (Courtesy C. P. Daghlian.)

on this fascinating subject, see the excellent compendium of papers in Krumbein et al. (2003a). Fossil deposits which show a great diversity of organisms preserved, or excellent preservation, or both, are called Lagerstätten (sing. Lagerstätte). Lagerstätten of various ages have provided paleobotanists with a wealth of information on plants of the past (see, e.g., Chapter 6). ELECTRON MICROSCOPY Scanning electron microscopy (SEM) has become a commonly used research tool in paleobotany to illustrate pollen grains and plant cuticles, because of the extensive range of magnifications available (up to 100,000 times) and the extreme depth of focus that can be achieved. In some instances, compressed leaf surfaces and various structures on them (e.g., stomata and trichomes) can be examined directly with the SEM (FIG. 1.28). In other cases, it is necessary to make latex replicas of the plant surfaces in order to interpret complex structural details. TEM has also been employed in the study of fossil plant cuticles. For TEM studies the plant cuticle is embedded in an appropriate embedding medium (e.g., Spurr epoxy resin), sectioned on an ultramicrotome, and stained in much the same way as living plant tissues are prepared for ultrastructural examination. Many fossil cuticles reveal lamellae and delicate structural features similar to those in modern cuticles (Archangelsky and Taylor, 1986; Guignard and Zhou, 2005). Varying patterns in the ultrastructure of cuticle from the same leaves have been documented and suggest that such differences may reflect cuticle from sun and shade leaves (Guignard et al., 2001). In addition,

CONFOCAL MICROSCOPY Recently, three-dimensional confocal laser scanning microscopy (CLSM) has been added to the arsenal of tools used by paleobotanists to extract information from the fossil record (Schopf et al., 2006). This technique utilizes a sequence of closely spaced images that can provide information in three dimensions. The technique is non-destructive and noninvasive, and has been successfully applied to Precambrian microscopic fossils in order to characterize not only morphology, but the nature of the preservation, including possible cell contents. Because the specimens examined must provide an autofluorescent signal, the fossils cannot have been geochemically altered. Like many techniques used in paleobotany, the procedure needs to be investigated on a particular fossil and, if the desired information cannot be obtained, the investigator needs to modify the technique or explore another means of obtaining the information needed. MACERATION AND DÉGAGEMENT Doran (1980) employed a bulk maceration technique to study Devonian compression fossils that were preserved in a silicified tuff matrix. He submerged the rock in hydrofluoric acid (HF) until the fossils were freed from the matrix. This technique provided nearly complete plants, and Doran could thus more accurately reconstruct the complete morphology of the plants. This method is useful because plant axes that extend into the matrix can be totally freed, but it only works on material where enough organic matter is preserved for the plants to remain intact through the maceration process. A more widely used technique to uncover compressed plant parts within the rock matrix is dégagement. This technique was developed primarily by Suzanne Leclercq (1960) and involves removing the rock matrix—often grain by grain— using fine steel needles (FIG. 1.29).

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paleobotany: the biology and evolution of fossil plants

valuable for studying specimens preserved in highly metamorphosed shales where much of the specimen is covered by the matrix and where bedding planes are poor. This technique not only provides details that cannot be obtained with conventional techniques but also makes some threedimensional reconstructions possible through the use of stereoscopic X-ray analysis. Uncovering the three-dimensional nature of fossil plant parts that are compressed or otherwise encased in the rock matrix is a goal in many paleobotanical studies. More recent improvements in the capture and analysis of X-ray images suggest that this technique will be more widely used in paleobotany in the future (Dietrich et al., 2000). X-ray computed tomography (CT) scans have been widely used in medicine, and vertebrate paleontologists have adapted these methods, using high-resolution scans (HRXCT), as a non-destructive method to produce three-dimensional images of vertebrate bones (Conroy and Vannier, 1984). Only recently, however, these methods have been used on fossil plants. Devore et al. (2006) used HRXCT to image the morphology and anatomy of pyritized fruits and seeds from early Eocene London Clay Formation. Because fossils preserved the in pyrite are fragile and deteriorate over time if exposed to air, they are conserved by placing them in sealed tubes of silicon oil. Using HRXCT it is possible to examine the fossils without removing them from the vials, thus decreasing the chances of exposing the specimens to air and subsequent deterioration. This technique makes it possible to study type specimens non-destructively and to reexamine characters that were initially used to define taxa and to evaluate forms for which the taxonomic affinities remain equivocal. It also preserves the integrity of the fossils so that they may be utilized in subsequent studies, perhaps when other, newer techniques are developed (Matysová et al., 2008). COAL AND CHARCOAL

Figure 1.29 Impression-compression of stem surface of Colpodexylon deatsii (Devonian). Bar ⫽ 2 cm.

OTHER TECHNIQUES Although X-ray analysis has been used for many years by paleontologists working with animal fossils, historically this technique has been little used for fossil plants (Stürmer and Schaarschmidt, 1980). X-ray analysis has been especially

Technically, coal (FIG. 1.30) comes under the definition of a compression fossil, since it represents a complex, heterogeneous mixture of macromolecular organic compounds derived from plant material that has been compressed over time (Scott, 1987). In general, the lower the rank of the coal (the degree of coalification), the more details of plant structure one can observe. The higher the rank, the more the coal has been metamorphosed and the higher the carbon content. Ranks from lowest to highest are lignite, subbituminous coal, bituminous coal, and anthracite. Lignite represents an early stage in coal formation, so the plant parts within lignite are not excessively crushed or decayed and are generally easily recognizable. In some instances, SEM has been a

chapter 1 introduction to paleobotany, how fossil plants are formed

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Figure 1.30 Exposure of coal in Antarctica (Permian). Ham-

mer ⫽ 30 cm.

useful tool in identifying plant parts preserved in lignites (Alvin and Muir, 1969). In some lignites it is possible to tease apart the plant fragments and make whole mounts of various structures, for example in the Brandon lignite, a famous early Miocene plant locality in Vermont, USA (Haggard and Tiffney, 1997). Bituminous coal is more metamorphosed and the plant parts are more flattened, but it is still possible to study plant fragments within the coal. Anthracite coal, the most highly metamorphosed type, is altered to such an extent that little of the original plant material is recognizable. Some coals can be thin sectioned for microscopic examination, and pollen grains, spores, and fragments of cuticle can be discerned. In other instances it is possible to coat the polished surface of coal with epoxy resin and etch it in a low-temperature plasma asher (Winston, 1989). Pieces of coal, or peels of the etched surfaces, can then be examined by light microscopy or SEM to determine the biological composition of the coal. This procedure makes it possible to quantify the plants in various types of coals in instances where coal ball permineralizations (see section “Cellular Preservation”) are not available (Winston, 1986). Coal can also be macerated using chemicals that break down the solid coal and release the plant fragments. It is possible to recognize cuticle, pieces of bark, bits of wood, solidified resins, and especially spores and pollen grains in this type of preparation. Examination of these components allows one to determine the kinds of plants that were growing in the ancient swamps where the coal was formed. Application of 13C nuclear magnetic resonance (NMR) and pyrolysis–gas chromatography–mass spectrometry techniques has been used to define stages in the coalification process more accurately (Hatcher et al., 1989). This same technique has also been used for Cenozoic

Figure 1.31 Marie C. Stopes.

leaf tissues and wood to identify various biomolecules (Yang et al., 2005). The components of coals can also be useful in documenting paleoecology (Poole et al., 2006). Macerals are defined as the organic constituents that comprise coal as seen in polished thin sections. The system of maceral types was originally proposed by the paleobotanist Marie C. Stopes (FIG. 1.31) in 1919, expanded in 1935, and is constantly kept up to date (ICCP, 2001). Maceral names end in -inite; for example, funginite is made up of fungal spores and various fungal bodies, secretinite is composed secretory deposits formed by medullosan seed ferns (Lyons, 2000), and sporinite consists of the sporopollenin walls of fossil pollen and spores. More detailed studies of coal composition provide valuable information about environmental parameters. For example, G. Taylor et al. (1989) suggested that the association of alginite and inertodetrinite (redeposited small particles of fusinite) in the Permian coals of Australia indicates a paleoenvironment of wet, cool summers and freezing winters. It is possible to distinguish between angiosperm and gymnosperm woods in some coals using macerals (Sýkorová et al., 2005). Fossil charcoal or fusain (carbonaceous residue that results from the incomplete combustion of organic material;

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paleobotany: the biology and evolution of fossil plants

also called fusinite) is also an important source of paleobotanical data (Cope and Chaloner, 1985; Lupia, 1995), with charcoalified plant remains dating back to the earliest land plants (Glasspool et al., 2004b). There are several techniques used to examine fossil charcoal (Sander and Gee, 1990; Guo and Bustin, 1998; Figueiral et al., 2002) which provide information on taphonomy and paleoecology (Scott et al., 2000), including past atmospheric composition (Scott and Glasspool, 2006) and the presence of fire in paleoecosystems (Uhl et al., 2004, 2007a; Collinson et al., 2007). The discovery of beautifully preserved charcoalified flowers in Cretaceous (Tiffney, 1977; Friis and Skarby, 1981) rocks from around the world has contributed large amounts of information to our knowledge of early flowering plants (see Chapter 22). In North America, Carboniferous coals of different ages are typically characterized by the dominance of different types of swamp plants (Cross and Phillips, 1990). Among the Pennsylvanian coal beds for example, lycopsids, tree ferns, calamites, seed ferns, and cordaites constitute the major types of tropical–subtropical arborescent plants that contributed to the peat formation. Although Carboniferous peat swamps have represented the model system in most interpretations of coal-forming ecosystems, the plants lived in atypical terrestrial communities in which the pH and available nutrients were low. It is now becoming apparent that such factors as types of litter accumulation, nature of the biomass, preservational characteristics of certain tissue systems, microbial diversity, biology of the plants, paleoclimate, and paleogeography are but a few of the parameters necessary to understand and properly interpret coal-forming ecosystems through geologic time (Cross and Phillips, 1990; DiMichele et al., 2002, 2007a). An important study by Gastaldo et al. (2004) underscores the fine resolution needed to understand fossil plant community structure, using an in situ three-tiered forest above a Pennsylvanian coal in Alabama, USA, as the data set. Detailed sampling of this fossil forest indicated that the proportion of canopy, understory, and ground-cover plants was variable across the study area, and that wet–dry gradients and/or increasing habitat specialization did not control the distribution of the plants species in this swamp ecosystem. In rare instances, a coal is formed that consists entirely of cuticular fragments and amorphic organic material (DiMichele et al., 1984). The cuticle is so abundant that it can be peeled off in thin layers. This type of coal is termed a paper coal, alluding to its papery appearance, and is known from relatively few localities, some as early as the Devonian, for example the famous Orestovia paper coal from Siberia

(Ergolskaya, 1936a; Krassilov, 1981a). It is a simple matter to isolate these cuticular fragments by using a chemical base such as potassium hydroxide. The cuticle can then be washed, stained in some cases, and mounted directly on slides for examination (DiMichele et al., 1984; Kerp and Barthel, 1993). Lenses of leaf fragments may sometimes be preserved within coals; these apparently formed in small depressions containing acidic water, which inhibited the normal degradation activities of various microorganisms (Gastaldo and Stub, 1999). In other instances, coals have been found to be made up exclusively of algal remains (see Chapter 4), some as early as the Precambrian (Tyler et al., 1957). Kerogen is a type of fossilized insoluble organic matter that is widely found in sedimentary rocks, and is a common component of various paleobotanical preparations. It is the most abundant form of organic carbon on Earth—more even than coal deposits. The presence of kerogen in rocks has been used as evidence of some of the earliest life on Earth (Moreau and Sharp, 2004; see Chapter 2). Understanding the chemical composition and source of kerogen, termed “typing” the kerogen, is especially important, since these factors help to determine the petroleum-generating potential of source rocks. In the past, kerogen and coal were generally analyzed using just thin sections and light microscopy. Today, both substances are also characterized using standard geochemical methods, such as pyrolysis, gas chromatography– mass spectrometry (GC–MS), analysis of carbon isotopes for total organic carbon (TOC), and others. There are a variety of other techniques available today to investigate the nature of the organic matter that remains after fossilization and to compare the carbonaceous residue to determine the chemical-structural characteristics. Raman spectroscopy has been used to characterize carbonaceous matter in highly metamorphosed rocks for some time (Nestler et al., 2003), but has recently been applied to microscopic fossils preserved in chert of varying ages (Schopf et al., 2005). Unlike most geochemical techniques, Raman spectroscopy is a non-destructive means to analyze ancient organic matter. It provides information on the original biochemistry of the organism, and can help resolve the nature of certain ancient fossil-like organisms (see Chapter 2). Another approach that has been used to examine the chemical composition of fossil plant materials involves energydispersive X-ray microanalysis (EDXMA). With this technique the elemental composition and spatial distribution of fossils can be studied without damaging the specimen (Briggs et al., 2000). Other have used EDXMA to map the distribution of elements in fossil cells (Boyce et al., 2001), and cell walls (Boyce et al., 2002).

chapter 1 introduction to paleobotany, how fossil plants are formed

Figure 1.32

Impression specimen of Osmunda claytoniites from Triassic of Antarctica. Bar ⫽ 2 cm.

Figure 1.33

Impression of several whorls of Annularia stellata leaves (Pennsylvanian). Bar ⫽ 1 cm.

IMPRESSIONS

When a paleobotanist splits a rock that contains fossil plant fragments along a bedding plane, it is sometimes possible to see the carbonaceous film of a compression along one face, and a negative imprint of the plant part, with little or no carbon adhering, on the other face (FIG. 1.32); these two faces are called part and counterpart in paleobotany. The fossil with little or no carbonaceous material is called an impression

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Figure

1.34 Impression of Sigillaria leaf bases showing parichnos scars and position of leaf trace (Pennsylvanian). Bar ⫽ 1 cm. (Courtesy BSPG.)

(FIGS. 1.33, 1.34). The imprint will show all the surface details of the compression, such as leaf shape and venation, but there is no actual plant material, that is no carbon, preserved. If you have ever seen a leaf imprint in a concrete sidewalk, you have seen an impression. The process involved in the formation of an impression is also analogous to these modern “fossils.” Such imprints are formed when leaves fall and settle into the wet concrete just after it is poured. As the concrete hardens, it conforms to the contours of the lower side of the leaf that rests on it. Eventually, the leaf disintegrates and the pieces are blown away, but a negative replica of the leaf remains on the hardened concrete. If you have ever put your initials in wet concrete, you have formed an impression. The impression of dinosaur footprints represents an excellent example of this type of fossilization process. When several footprints are of the same type or a series of trackways are discovered in close proximity, it may be possible to extrapolate the stride of the organism and, from this, infer something of the biomechanics of the animal. No cellular details can normally be seen on an impression because there is no adhering organic material, but, in some instances, especially where the matrix is exceedingly fine grained, a replica of the impression can be made with latex or similar material. The replica faithfully reproduces whatever surface details were on the original organism when it was impressed into the mud. Examination of part of the replica with the SEM may reveal details with great clarity, such as the pattern of the epidermal cells, hairs, glands, or other surface features. Some impression fossils are covered with mineral encrustations of different composition, for example iron (Spicer, 1977). These deposits may be the result of the

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paleobotany: the biology and evolution of fossil plants

Figure 1.35 Cast of large seed fern seed (Pennsylvanian).

Bar ⫽ 2 cm.

activities of microorganisms during the decay process. Regardless of their origin, however, the mineral crust may provide an excellent replica of the surface of the plant part, and this can be studied using a variety of imaging modes. MOLDS AND CASTS

In addition to two-dimensional plant parts, such as leaves, three-dimensional structures, such as stems, seeds, or fruits, can also be carried into sites where sediment is accumulating and buried. During flood events, massive trunks and tree branches can be moved some distance before they are eventually deposited. If these plant parts became crushed over time, they would be preserved as compression or impression fossils. If, however, the sediment surrounding the threedimensional plant parts hardens before the plant fragment is crushed, the sediment will form a three-dimensional negative, or mold, of the plant fragment. As the plant material disintegrates, a hollow remains in the sediment, which can subsequently be filled in with sediment, thus forming a cast inside the mold. The surface of the cast and the mold can often faithfully reproduce the surface features of a particular plant part, such as characteristic leaf bases on the surface of a stem or the ornamentation of seeds (FIG. 1.35) and fruits. The sediment that fills in the cavity of the mold and solidifies becomes a three-dimensional cast of the original plant part

Figure 1.36

Cast of arborescent lycopod (Protostigmaria eggertina) (arrows) (Mississippian). Hammer ⫽ 15 cm.

(FIG. 1.36). In almost all molds and casts no actual plant material remains, but the surface contours are the same as those of the original plant part. The formation of fossil molds and casts parallels the method by which a sculptor creates a bronze statue. The sculptor does not carve directly on a block of bronze, but creates a sculpture with some other medium— wood or wax perhaps. A mold is then constructed around the original sculpture and, when the mold is complete, the original is removed in some fashion (disassembling the mold temporarily or melting the wax). When the mold is reassembled, molten bronze is poured into it, and an exact replica of the original sculpture (but one that involves none of the original material in that sculpture) is formed. Rates of sedimentation in certain areas where molds and casts were formed must have been spectacular. As an example, the sea cliffs at Joggins, Nova Scotia, reveal exposed casts of Pennsylvanian tree trunks 3–8 m tall. The trees must have been buried quite

chapter 1 introduction to paleobotany, how fossil plants are formed

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Figure

1.37 Compressed trunk cast of Eospermopteris (Devonian). (Courtesy W. E. Stein.)

Figure 1.39 Cast of several tracheids showing circular bor-

dered pits (Miocene). Bar ⫽ 55 μm.

Figure 1.38

Large pith cast of Calamites close to the insertion to a rhizome (Permian). Bar ⫽ 20 cm.

rapidly in place. Sediment hardened and the trees subsequently died, leaving hollows (molds) in the hardened rock that were subsequently filled with other sediments (casts). Compressions, and casts (FIG. 1.37) are important in showing the external form of plant parts in a three-dimensional fashion. Root casts of trees can provide important morphological information useful in determining the type of soil formation and soil drainage conditions when the plants were growing (Retallack, 1990). They also may reveal specialized taphonomic processes and how degradation of organic tissues may have proceeded (Driese et al., 1997). A special form of cast is the calamite pith cast or steinkern, which is a common form of preservation of larger calamite stems and branches. Pith casts are casts (FIG. 1.38) of the hollow pith or medullary region in calamites and

preserve an impression of the outside of the pith cavity, which represents the inside of the vascular tissue and cortex (see Chapter 10 for further details). An unusual example of a mold and cast is represented by fossil wood that was exposed to colloidal silica during the diagenesis; the silica permeated the cell cavities, but somehow did not impregnate the cell walls. After precipitation of the silica within the cell cavities, the cell walls (⫽molds) disintegrated and all that is left are casts of the cavities of the wood cells (FIG. 1.39). These cell casts have the negative contours of the insides of the cell walls and show counterparts of specialized wall structures, such as bordered pits (Chapter 7). CELLULAR PRESERVATION

With few exceptions, none of the preceding types of fossil preservation provide the opportunity to examine the internal structure of a plant or plant part. In the case of permineralizations and petrifactions, however, it is possible to study the internal anatomy of ancient plants (Schopf, 1975). In these fossils, one can examine cells and tissue systems within a plant, as well as produce a series of serial sections that can be used to reconstruct the three-dimensional organization of a structure. This type of fossil is called a permineralization or a petrifaction.

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paleobotany: the biology and evolution of fossil plants

Figure 1.40 Several silicified logs in the petrified forest of Patagonia, Argentina. S. Archangelsky, left and T. Delevoryas, right.

In both types, the process begins when a plant part becomes immersed in water containing a high concentration of dissolved minerals, the most common being silica (silicon dioxide, SiO2), which is often readily available in areas of volcanic activity. The plant part, for example a log, gets thoroughly waterlogged, with water and dissolved minerals permeating all the cells and tissue systems. The dissolved minerals may be silica compounds (silicification) (FIG. 1.40), carbonates (e.g., calcium carbonate, CaCO3), oxides, pyrites (iron sulfide, FeS2), or some other type of chemical. At this stage it is unclear what happens, but something triggers precipitation of the dissolved mineral (e.g., a change of pH) so that it hardens around and within the plant fragment. The cell walls of the plant itself may serve as nucleation sites for the growth of the mineral crystals. When the mineral is completely solidified, the plant fragment, in effect, is entombed within solid rock. The fossil can now be sectioned by various means and examined under the microscope to see internal details of the plant. Although several authors have attempted experimental silicification of wood in the laboratory (Leo and Barghoorn, 1976; Laroche et al., 1989), the preservation seen in fossils is often much better. Preservation of plants as petrifactions or permineralizations probably involves several stages of mineral growth, with different sizes of crystals involved. Some more recent work (Channing and Edwards, 2004) suggests that colloidal or gel phases of some minerals may be involved in the apparently rapid preservation of minute details. Permineralizations and petrifactions can both be studied by means of thin sections, sometimes called petrographic thin sections (FIG. 1.41) (Hass and Rowe, 1999). The piece of rock containing the fossil is cut and ground thin enough

Figure 1.41

Prepared commercial thin section by the James Lomax company of Carboniferous coal ball plants.

to transmit light through the section, essentially, the same technique that geologists use to make petrographic rock sections. Rock saws are available that can cut through most types of rock matrix; most have steel blades with diamond particles embedded in the cutting edges. Oil or some other coolant is used to keep the blade from getting too hot as it slices through the rock. Saw blades covered with or made of particles of silicon carbide or some other abrasive can be used to cut through softer material. The fossil to be studied is cut out with a saw, and the surface of the fossil is polished with an appropriate abrasive (e.g., silicon carbide of various grades) until it is smooth. The surface showing the fossil is then attached to a piece of glass with some type of adhesive. After the adhesive has solidified, the glass slide with the piece of permineralized material is placed back in a saw, now a specialized thin-sectioning saw, and the remainder of the rock is cut away to leave as thin a slice as possible. At this point, the rock is still opaque. The next step involves grinding the surface, either by hand on a lapidary wheel or plate, or on a thin-sectioning machine, so that more and more light can pass through the specimen. Eventually, the sliver

chapter 1 introduction to paleobotany, how fossil plants are formed

of rock is thin enough to be examined with a microscope. Sometimes the piece of glass to which the fossil material is attached is the actual slide used for study. In that case, a permanent adhesive, such as epoxy resin, may be used. Some prefer to transfer the ground specimen to a clean microscope slide. In those instances, a cement that can later be remelted is used, such as Lakeside thermoplastic resin. Before the thin section is transferred, it is coated with a transparent plasticlike material to keep the section intact. This thin slice is then placed on a clean slide with a natural or synthetic mounting medium and covered with a cover glass. Once the medium has hardened, the slide can be examined with a compound microscope. Some paleobotanists use no cover glass, but rather examine the rock surface directly using oil immersion microscope objectives; this method has been applied very successfully with the Early Devonian Rhynie chert (see Chapter 8). PERMINERALIZATION In a permineralization, minerals fill the cell lumina and the intercellular spaces, but do not completely replace the cell walls. The cell walls still consist of organic matter, although they may be chemically altered to various degrees. Chemically, the various layers of the cell wall may still be distinct (Boyce et al., 2002), and the permineralization may faithfully reproduce the microstructure of the wall, for example the position of cellulose microfibrils (Smoot and Taylor, 1984). Cellular contents have even been described from permineralizations! The processes involved in the formation of certain types of permineralization in silica are being studied in modern hot springs ecosystems like Yellowstone National Park, USA (Channing and Edwards, 2004), and in filamentous microbes from similar ecosystems in New Zealand (Renaut and Jones, 2003; Jones et al., 2004; Phoenix et al., 2005). These studies underscore the complexity of the preservation process. In general it involves the formation of opaline silica (opal-A) films that coat structures and colloidal silica that permeates cells and tissue systems. More recent work has shown that bacteria may be involved in or even necessary for many mineralization processes, and the field of geomicrobiology is a rapidly growing area of study. In biomineralization, the bacteria may serve as catalysts for chemical reactions and also as nucleation sites for mineralization (see Konhauser, 2007 for additional information on this topic). An analogy of the process of permineralization is the technique used to embed and section living biological material. For example, a piece of plant is killed and fixed in an appropriate chemical. It is then passed through a series of

25

alcohols to dehydrate the tissue, and finally transferred to molten paraffin or plastic. When the paraffin is cooled, the plant part is completely embedded in it—paraffin is present within the tissues as well as around them. The entombed specimens can then be serially sectioned to reveal details of the cells and tissue systems. PEEL TECHNIQUE. The peel or acetate peel technique (FIG. 1.42) is a simple and rapid method for preparing sections of permineralized plants (Joy et al., 1956; Galtier and Phillips, 1999). In order to use the peel technique, there must be a certain amount of organic matter still present in the cell walls of the fossil plant. If not, thin sections have to be prepared. The rock containing the fossil is sliced with a rock saw (FIG. 1.43) and the resulting slab is polished (FIG. 1.44), first with a coarse abrasive (100–400 grit size) on a lapidary wheel and finally with abrasive of progressively finer grain sizes (600 grit size). The polished surface is then ready to be etched. If the fossils are entombed in calcium carbonate (see coal balls below), etching is done in a dilute solution (⬃5%) of hydrochloric acid (FIG. 1.45). The acid reacts with the carbonate, but not with the organic remains, so the mineral material (CaCO3 in this case) is slowly etched away, leaving the plant cell walls (and cellular contents, if present) projecting in relief from the surface of the slab (FIG. 1.46); the etched surface should not be touched at this stage as the cell walls are very delicate. After the surface has been rinsed and air dried, it is ready to be peeled. Acetone, which is an organic solvent, is poured on the etched surface and, before it evaporates, a thin sheet of transparent cellulose acetate (or similar plastic) is carefully rolled on the surface (FIG. 1.47). The acetone will partially dissolve the lower surface of the acetate sheet, converting it to a liquid that flows in and around cell cavities and intercellular spaces. Because acetone is quite volatile, it evaporates readily, so the lower surface of the acetate sheet quickly solidifies, embedding the cell walls within it. When the acetate is completely dry, it can be pulled from the surface of the rock, taking with it a thin section of the entombed plant (FIG. 1.48). The greatest advantage of the peel technique is that serial sections can be made quickly down through the rock by polishing, etching, and repeating the process again and again (FIG. 1.49). The peel technique (Stewart and Taylor, 1965) can be used for different types of permineralizations, but when the matrix is something other than a calcium or magnesium carbonate, a different acid or a different concentration of acid must be used. When the peel technique was first devised, preformed sheets of cellulose acetate were not available; rather, a solution of parlodion, butyl acetate, amyl alcohol, xylene,

26

paleobotany: the biology and evolution of fossil plants

Figure 1.42

Diagrammatic representations of the steps involved in the preparation of the coal ball peel technique. A. Section of coal ball slab (calcium carbonate matrix) containing plant material (crosshatched); B. coal ball slab after acid etching to partially expose plant material; C. etched coal ball slab surface with cellulose acetate sheet in place; D. cellulose acetate sheet (peel) being pulled from the surface with adhering plant material; and E. coal ball peel containing embedded plant material. (From Taylor and Taylor, 1993.)

Figure 1.44 Figure 1.43 Several pieces of coal ball after sectioning.

abrasive powder.

Polishing the coal ball slab on a glass plate using

chapter 1 introduction to paleobotany, how fossil plants are formed

27

Figure 1.45 Etching the coal ball slab in dilute hydrochloric

Figure 1.48 Removing the peel from the coal ball slab

acid.

surface.

Figure 1.46 Etched surface of coal ball slab prior to flooding

the surface with acetone.

Figure 1.49 Coal ball peel, left, and coal ball slab at right

from which it was removed.

castor oil, and ether was poured on the surface and allowed to dry (Darrah, 1936) (FIG. 1.50). This resulted in peels that were not uniform in thickness and were sometimes difficult to mount on microscope slides. Another drawback was the amount of time required for the poured peels to dry on the coal ball surface, as compared with the approximately 20 min required for cellulose-acetate-sheet peels to dry. Despite these drawbacks, the poured peels may still be useful, especially when examining very delicate structures and surfaces that are irregular.

Figure 1.47

Rolling the acetate sheet into position on the coal ball slab. Bottle contains acetone.

COAL BALLS. We know more about the anatomy, morphology, and biology of Carboniferous coal-swamp plants than those from any other time period, and this is primarily due to coal balls. During the Carboniferous, North America

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paleobotany: the biology and evolution of fossil plants

Figure 1.52

Digging coal balls from a stream bank in Illinois,

USA.

Figure 1.50 William C. Darrah.

Figure 1.53 Transporting bags of coal balls from a site in

Kentucky, USA.

Figure 1.51 Collecting coal balls at a strip mine in southern

Illinois.

and Europe were close to the equator and contained extensive tropical forests which contributed to the extensive coal deposits characteristic of these areas today. Associated with some of these coal deposits are coal balls (FIGS. 1.51–1.53), variously shaped nodules which occur in bituminous coal seams. Coal balls represent permineralized peat deposits and are composed almost entirely of plant parts preserved in calcium carbonate. Some of the first ones found in England

were nearly spherical, hence the name, coal ball, but they can be irregular in shape and range from a few centimeters across to many meters in thickness. Some of the oldest ones come from the upper Namurian (Upper Mississippian) of Germany and the Czech Republic, but they are also known from Permian coal deposits in China. They can be readily studied by means of the peel technique. The method of formation of coal balls has been examined by a number of paleobotanists (Falcon-Lang, 2008), beginning with Stopes and Watson (1908), but the process is still not fully understood. When fresh or partially decayed, the peat was infiltrated by carbonates (fibrous calcite) before there was extensive compaction of the plants within. Since some coal balls are associated with marine limestones, it has been suggested that the plants were growing in lowlying, swampy areas close to the sea, and this hypothesis fits

chapter 1 introduction to paleobotany, how fossil plants are formed

with the paleogeography of Midcontinent North America during the Carboniferous. During storms or marine transgressions (Mamay and Yochelson, 1962), the coal swamp was inundated by seawater, which provided a source of calcium carbonate for permineralization. This hypothesis explains the mixed nature of some coal balls in which both plant and marine animal remains are preserved. Scott and Rex (1985) suggested that all coal balls are not formed by the same process and put forward a non-marine model of formation in which the permineralizing fluids are derived from percolating groundwater high in carbonates. Scott et al. (1996) examined the origin of Carboniferous and Permian coal balls from Euramerica and China and concluded that several different mechanisms were involved, depending on the region and the location of the coal balls within the coal seam. Based on carbon isotopes, they found that some coal balls involved a mixture of marine and meteoric fresh water percolating through the peat and noted that most coal balls formed in freshwater basins with at least some marine influence. There can be little doubt that the formation of coal balls was a highly specialized process, as none are known after the Carboniferous–Permian. To the coal miner these calcium carbonate coal balls represent impurities in the coal that are often termed “fault,” but to the paleobotanist they provide a source of fascinating information that can be used to investigate the biology of the plants that lived in the peat swamps hundreds of millions of years ago. OTHER PERMINERALIZATIONS. Many permineralizations contain silica as the embedding mineral (FIG. 1.54). In fossil peat from Permian and Triassic rocks (FIGS. 1.55, 1.56) from the central Transantarctic Mountains of Antarctica, the silica is in the form of chalcedony (Schopf, 1971). It is possible to make acetate peels of silica permineralizations; however, they must be etched in concentrated HF. When using HF, precise safety procedures (e.g., etching in a fume hood, proper gloves and other protective clothing, and eyewear) must be employed because of the very dangerous nature of this acid. In some cases, especially in certain Devonian fossils, preservation involves permineralization via pyrite (iron sulfides) or limonite (hydrated iron oxides). Plant parts preserved by these minerals have been difficult to study because the material often breaks apart during grinding and is lost. To eliminate such problems, specimens of this type need to be first embedded in plastic prior to cutting (Stein et al., 1982). For fossils preserved in ironstone (fine-grained sedimentary rock), a useful technique involves selectively macerating the specimen in acid to free the silicified axes and then embedding the

Figure 1.54

29

In situ stump of Triassic tree in Antarctica. Yellow

pen for scale.

Figure 1.55

Block of Triassic chert (orange color) from

Antarctica.

axes in bioplastic to examine internal anatomy (Aulenback and Braman, 1991; Serbet and Rothwell, 2006). The degree of detail that can be preserved by permineralization is truly extraordinary, with such delicate structures

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paleobotany: the biology and evolution of fossil plants

Figure 1.58 Spores of Cyathotheca tectata showing distal (left) and proximal surfaces, and distinct ornamentation (Pennsylvanian). Bar ⫽ 18 μm. Figure 1.56 Block of permineralized peat from Antarctica showing root of Glossopteris, with wood wedges alternating with lacunae, Vertebraria (Permian). Bar ⫽ 2 cm.

Figure 1.57 Two animals (Ebullitiocaris oviformis) (arrows)

attached to an Aglaophyton major stem (Devonian). Bar ⫽ 0.5 mm. (Courtesy H. Kerp.)

as starch grains, nuclei, various types of membranes, tapetal deposits, and cells of seed-plant microgametophytes are known. Spores of lycopsids and microspores of Pentoxylon have been interpreted as containing chromosomes (BrackHanes and Vaughn, 1978; Bonde et al., 2004). The flagellum of a chytrid zoospore (FIG. 3.20) (Taylor et al., 1992) and rotifers (FIG. 1.57) from the Rhynie chert, and sperm within the pollen chamber of a Permian seed (Nishida et al., 2003) have been described from permineralized plant remains. There are numerous examples of exceptionally well-preserved plant structures throughout this book.

In some instances, the matrix of the permineralization is too crumbly to allow preparation of ground thin sections or does not lend itself to the peel technique. In such cases, it may be necessary to examine the cut and polished surface with reflected light. If a series of sections is necessary, one must make a photographic record or a series of drawings, because the specimen will be lost as it is continually ground away, leaving no actual record of each face examined. PETRIFACTION Cellular details can also be observed in a petrifaction. In this case, all of the original organic matter in the plant has been replaced by minerals. Many fossil woods, such as those from the Triassic Petrified Forest in Arizona and the Cerro Cuadrado (Jurassic) Petrified Forest in Patagonia, Argentina (FIG. 1.40), are preserved in this manner. It is necessary to make thin sections to study petrifactions, since the etching involved in producing a peel preparation would completely dissolve the specimen. Other techniques such as cathodeluminescence are providing a new source of information about silicified wood (Matysová et al., 2008). UNALTERED PLANT MATERIAL

Some plant parts are found as fossils in an unaltered form, either as body fossils or as chemical fossils. Pollen grains and spores (FIG. 1.58), diatom frustules, cuticle envelopes, various types of resins, such as amber (FIG. 1.59) and calcium carbonate remains of certain types of algae are all examples of unaltered plant fossils. In some instances even the soft parts are sufficiently preserved so that comparisons can be made at the cytoplasmic and ultrastructural level (Wolfe et al., 2006). Holocene peat is an example of relatively unaltered plant material (Williams and Yavitt, 2003). Plant parts became

chapter 1 introduction to paleobotany, how fossil plants are formed

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Figure 1.59

Stamen (arrow) embedded in amber in the process of shedding pollen as it was being preserved (Miocene). Bar ⫽ 1 mm. (Courtesy G. O. Poinar.)

Phytolith of a dicot (Oligocene). Bar ⫽ 20 μm. (Courtesy C. A. E. Strömberg.)

Figure 1.61 Phytolith (laminated trichome-type) from a dicot (Eocene). Bar ⫽ 30 μm. (Courtesy C. A. E. Strömberg.)

Figure 1.60

incorporated into peat bogs, and because of the high acidity in the bogs, microbial activity is greatly reduced, so little or no decomposition occurs. The accumulated plant debris may build up to a considerable thickness, and while there is some disassociation of plant parts as well as flattening, the bits and pieces preserved can be handled like the same parts of modern plants. Another excellent example of unaltered plant material is diatomaceous earth. Although the cell contents are no longer present, the silica cell walls remain intact and are preserved in such fine detail that the exquisite sculpturing can be easily detected on the surface. Phytoliths also represent unaltered plant material secreted by the living plant in the form of calcium carbonate or opaline silica (FIGS. 1.60, 1.61). They occur in various types

Figure 1.62 Phytolith (echinate sphere-type) from a palm (Eocene). Bar ⫽ 15 μm. (Courtesy C. A. E. Strömberg.)

of grasses and some trees and, depending upon the species, vary in morphology and size (FIGS. 1.62, 1.63). Although they have been used for many years to study Holocene or Pleistocene habitats, recent research has utilized these plant markers to study older paleoenvironments. They have been especially useful in the interpretation and reconstruction of grassland ecosystems (Strömberg, 2004). Extracting fossil phytoliths can be accomplished using a variety of techniques (Parr, 2002), but it is important to avoid methodological bias, as discussed in Strömberg (2007, 2008). Spores and pollen grains are represented in the fossil plant record in great abundance because the wall (sporoderm) of

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paleobotany: the biology and evolution of fossil plants

Figure 1.63 Phytolith consisting of epidermal long cells with papillae and a row of short, siliceous vertical cross cells from a grass (Cretaceous). Bar ⫽ 50 μm. (Courtesy C. A. E. Strömberg.)

the spore or pollen grain is composed of an especially resistant material called sporopollenin. As such they also represent unaltered plant material. Spores and pollen grains may be common in certain rocks, even when there is no evidence of any other plant parts. It is possible to extract these pollen grains and spores from the rock and mount them on microscope slides. TEM has provided a wealth of new information about fossil pollen and spore walls that has been used to examine the development of the pollen wall (Taylor and Alvin, 1984). More recently, Scott and Hemsley (1991) have discussed the value of laser scanning and scanning acoustic microscopy in the study of paleobotanical materials. CHEMICAL FOSSILS Chemical fossils can also represent a type of unaltered plant material (Hemsley et al., 1996). Chemical signatures, sometimes called biomarkers or geomolecules, are specific for certain groups of organisms. These biomolecules are transformed through time with lipids perhaps having the best opportunity of being preserved (Itihara et al., 1974), whereas nucleic acids degrade more rapidly (Briggs et al., 2000).

Biomarkers in the form of terpenoids have recently been reported in the fossil wood type Protopodocarpoxylon from the Jurassic of Poland (Marynowski et al., 2007). An example of chemical preservation is the presence of hydrocarbons within Ordovician oil deposits that are known to be produced only by the putative cyanobacterium Gloeocapsomorpha (Hoffman et al., 1987; Foster et al., 1989; 1990; Blokker et al., 2001). Pristanes and phytanes are also a type of biomarker. These molecules are believed to be derived principally from chlorophyll degradation, but can also be produced by non-photosynthetic organisms (Hahn, 1982). A number of new techniques have been added to the arsenal of the paleobotanist, and these promise to provide significant advances in a number of areas. They include elemental analysis, chemolysis, pyrolysis, and lipid analysis, and have been used to study a large number of organic compounds throughout the geologic column. Pyrolysis and chemolysis have been used to screen for the chemical composition of the fossil material. Such procedures and techniques have increasing application in determining the systematic affinities of a particular organism, as well as determining various taphonomic processes that may have altered the fossil. These various paleobiochemical techniques involve the extraction of organic constituents still associated with the fossil or represented as residues in the rock matrix. Classes of chemical compounds, such as sterols, aromatics, carboxylic acids, polysaccharides, various types of lignin, fatty acids, and nalkanes, are but a few of the chemical constituents that have been identified in fossil plants. Organic chemical profiles have been used effectively with extant angiosperms and, at one time, chemosystematics represented a basic and almost routine technique in plant systematics (Crawford, 1990). These techniques have sometimes been applied to the study of fossil plant systematics, but it is important to consider diagenetic changes, especially in older fossils. Niklas et al. (1985) used steroid and other cycloalkane–alkene profiles to show that a Miocene Liriodendron leaf was chemotaxonomically more similar to one particular living species despite the fact that the fossil shares morphological characters with two living species. More recently, Mösle et al. (2002) demonstrated that the biomolecular cuticle signature was more comparable between more closely related plants, such as Cordaites and Walchia, than between these seed plants and certain coeval seed ferns. There are, however, certain limitations to such paleobiochemical approaches. For example, various microbial activities may alter the organic chemicals shortly after the organism dies, or there may be modifications to the chemical constituents as a result of diagenesis. Some organic compounds may have formed abiotically, rather than

chapter 1 introduction to paleobotany, how fossil plants are formed

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representing the original chemical constituents of the plants. Still others may have percolated through the surrounding rocks and constitute contaminants, even in rocks as hard as cherts. Thus, for paleobiochemistry to be useful to paleobiologists, analyses must follow strict qualitative and quantitative protocols that can be standardized and repeated (Van Bergen, 1999). ANCIENT DNA During the last two decades, systematists working with extant plants have switched, in part, from secondary metabolites to the use of molecular sequences, including nuclear, chloroplast, and mitochondrial DNA, as the macromolecules of choice in developing phylogenetic hypotheses for plant relationships. Golenberg and colleagues (1990) reported the extraction and amplification of an 820-base-pair DNA fragment from the chloroplast rbcL gene (ribulose-1,5bisphosphate carboxylase–oxygenase or RuBisCO) of a Magnolia latahensis leaf. The leaf was collected from the famous mid-Miocene (Langhian) Clarkia beds of northern Idaho, which are dated at 15–15.5 million years old (Ma). In another study on fossils from the same site, Kim et al. (2004) reported amplified ndhF (NADH dehydrogenase) from the same type of leaf (M. latahensis), and rbcL from a specimen of Persea, further suggesting long-term preservation of ancient plant DNA. Recently, however, these studies and others, including DNA sequences from bacteria in insects in amber, DNA in dinosaur bones, and in salt crystals have been challenged on various grounds. As a result some believe that DNA in excess of 1 million years old is probably an artifact (Pääbo et al., 2004). Others believe the study of ancient DNA holds promise at some level (Gugerli et al., 2005), but that the evidence must be compelling, and from multiple sources. Obviously, additional samples from the same site that demonstrate similar results will help verify such reports, and also a closely followed set of protocols will be especially useful in demonstrating the authenticity of ancient DNA (Gilbert et al., 2005). Although barely classified as ancient, an interesting study has recently reported 1000-year-old DNA from excavated wood samples using a strict set of procedures to insure that the material was not contaminated (Liepelt et al., 2006). MUMMIFICATION When conditions of burial are rapid, and especially in very dry or cold environments, wood or other plant parts may survive for millions of years in a relatively unaltered condition. Such mummified remains have been described from Cenozoic deposits (Basinger et al., 1988; Francis and Hill,

Figure 1.64

Mummified leaf of Cryptocarya (Lauraceae) (Eocene). Bar ⫽ 2 cm. (Courtesy D. C. Christophel.)

1996; Fukushima et al., 1996) and represent a special preservation type in which the plant tissue was rapidly dehydrated and buried (FIG. 1.64). So well preserved are the cells and tissue systems of these mummified plants that they can be studied by the same techniques as those used to examine extant tissues. Mummified wood is not mineralized, so it can be sectioned using techniques identical to those utilized by wood anatomists for extant material. AMBER Another example of unaltered plant material is amber (FIG. 1.65), a name typically applied to a wide variety of fossilized plant resins (Rice, 1987). Amber has been found in rocks from the Carboniferous to the Pleistocene, but most deposits have been reported from Cretaceous and Cenozoic strata. In the authoritative text, Plant Resins, Langenheim (2003) restricted the term amber to a lipid-soluble mixture of terpenoid or phenolic compounds, distinguishing it from gums, waxes, mucilage, oils, and latex. Amber is produced by a

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paleobotany: the biology and evolution of fossil plants

the original plant part, but may contain some components of the original plant. Certain types of algae are more common as fossils because they precipitate or bind calcium carbonate around or in their cells. This calcium carbonate skeleton can build up to a considerable thickness and provides excellent preservational potential. When the alga dies, the calcium carbonate skeleton persists, often for millions of years. Sectioning of these calcium carbonate residues allows one to reconstruct the three-dimensional appearance of the alga by following the configurations of the hollows within the calcium carbonate sheath. These limestone-precipitating algae play a very important part in the build up of some so-called coral reefs; in these cases, the bulk of the reef is produced by the accumulation of CaCO3 precipitated by algae, rather than by the corals living on the reef (see Chapter 4).

PALYNOLOGY Figure 1.65 Winged angiosperm seeds preserved in amber

(Miocene). Bar ⫽ 1 cm. (Courtesy G. O. Poinar.)

large number of plants; phytochemistry, infrared spectrophotometry, and X-ray diffraction have proved to be important analytical tools in determining the botanical origins of fossil resins (Langenheim, 2003). Because of its sticky consistency when it was produced by the plant, amber has also served as the fossilizing matrix for other organisms. In addition to pollen grains and other wind-borne microscopic plant parts, small flowers, fungi, a variety of insects (Peñalver et al., 2006), and other organisms are often preserved within pieces of amber. Even something as delicate as oil bodies in cells of liverwort leaves (Grolle and Braune, 1988), plant organelles such as chloroplasts and mitochondria (Poinar et al., 1996; Koller et al., 2005), a strand of spider silk (Zschokke, 2003), and amoebae (Schmidt et al., 2004) have been preserved in amber. Poinar (1992) provided an excellent historical account of amber, and the importance of this plant resin in examining the diversity of life preserved in this unique manner, and Grimaldi and Engel (2005) demonstrated the extraordinary preservation and diversity of insects entombed in amber in their comprehensive work, Evolution of the Insects. SUMMARY DISCUSSION

The preceding provided examples of the most common ways in which plants become fossilized, but there are other forms as well, or combinations of the preservational types just discussed. For example, some stem casts may contain a faint outline of the conducting system in the center of the cast. In this case, the cast is not simply a three-dimensional replica of

The science of palynology or, perhaps in a geologic context, paleopalynology is devoted to the study of pollen grains and spores, and also encompasses the investigation of other organic microfossils, such as chitinozoans, acritarchs (Javaux and Marshall, 2006), scolecodonts, dinoflagellates, certain types of microscopic algae, microforaminifera, rotifers, testate amoebae, chitinous fungal remains, and other forms of organic debris sometimes termed varia. Characteristic features such as grain shape (FIG. 1.58), wall sculpture, presence or absence of pores, ridges, furrows, or other types of structural features make it possible to distinguish among grains of various kinds and in some instances to assign them to certain groups of plants. The discipline of palynology is a critical component of understanding the biodiversity of the present and the past, and the important volumes by Wodehouse (1965), Erdtman (1969) (FIG. 1.66), Faegri et al., (1989) (FIG. 1.67), and Traverse (2007) (FIG. 1.68) provided an excellent historical context to the discipline. Palynology has greatly benefited from the introduction of various SEM techniques (Villar de Seoane and Archangelsky, 2008) that have made it possible to image and interpret complex external features on the grains (FIG. 1.69). There has also been an attempt to automate palynology, using texture analysis of SEM images (Langford et al., 1990; Vezey and Skvarla, 1990). This procedure greatly reduces the labor-intensive aspects of palynology and perhaps offers more rapid results, larger data sets, finer resolution of taxa, and possibly greater objectivity in identification (France et al., 2000). Fossil pollen grains and spores (FIGS. 1.70, 1.71) are now routinely sectioned and examined with the TEM as well.

chapter 1 introduction to paleobotany, how fossil plants are formed

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Figure 1.68 Alfred Traverse. (Courtesy M. Streel.) Figure 1.66 Gunnar Erdtman.

Figure 1.67 Knut Faegri (right) and Ove Arbo Høeg.

These studies have provided a wealth of detailed information about features of the exine (the outer spore or pollen wall that is composed of sporopollenin) that have been useful for systematic studies. Some paleobotanists have combined SEM (FIG. 1.72) and TEM studies of dispersed spores to try to better understand the affinities of these propagules (Edwards et al., 1996), and to more accurately interpret features of the wall (Wellman, 2001). Information on pollen and spore ultrastructure is often determined from single sections

Figure 1.69 Cyathotheca tectata spore viewed with the scanning electron microscope (Pennsylvanian). (From Taylor, 1972.) Bar ⫽ 23 μm.

of grains in which the plane of section is not easily determined, but techniques have been developed so that the same grain may be examined and recorded in transmitted light, and then scanning and TEM (Daghlian, 1982). In addition, it is often important to prepare serial sections of the same grain in order to view features, such as lamellae, that may not be consistently present throughout the entire wall (Johnson and Taylor, 2005).

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paleobotany: the biology and evolution of fossil plants

Figure 1.70

Ultrathin section of the spore Horstisporites iridodea showing organization of the sporoderm. Bar ⫽ 2.5 μm. Figure 1.72

Fractured surface of Cyathotheca tectata spore. Bar ⫽ 3 μm. (From Taylor, 1972.)

daunting, and some palynologists have developed automation techniques to assist in the process. For example, image analysis of measurements can be used to quantify shape and ornamentation on SEM images (Treloar et al., 2004). In a companion study, Li et al. (2004) used a neural network to analyze texture and were able to correctly identify four extant pollen taxa. GEOCHRONOLOGY AND BIOSTRATIGRAPHY

Figure 1.71

Ultrathin section of Cyathotheca tectata spore as viewed with a transmission electron microscope. (From Taylor, 1972). Bar ⫽ 12 μm.

Fossil pollen and spores that are preserved within the pollen sac or sporangium (in situ) can provide valuable information on developmental patterns in the formation of the pollen grain and spore walls. In certain types of fossils, such as permineralizations, it is possible to extract many pollen grains of the same type from a single sporangium, or from multiple sporangia at different stages of development. Study of these grains can thus offer insights into biological processes that took place millions of years ago (Taylor and Alvin, 1984). The process of identifying numerous palynomorphs, especially those that are dispersed (i.e., not in situ) can be

Perhaps the most widespread application of palynology is in geochronology, the dating of events in the history of the Earth. Palynomorphs and certain microfossils can be used in geochronology, that is, dating rock units. Fossils can only provide a relative date for strata, that is in relation to other units. Absolute dating relies on other methods to give a specific date (see radiometric). Dating with palynomorphs is possible because many change through time or possess unique features that allow them to be distinguished from other types. For example, Upper Cretaceous and lower Paleogene rocks in the Northern Hemisphere contain a unique type of fossil angiosperm pollen termed triprojectates (Farabee, 1990). These grains are unusual in that they possess polar and equatorial projections (FIG. 1.73) and a variety of ornamentation patterns that make them especially good biostratigraphic markers. Although the botanical affinities remain problematic, it has been suggested that at least some triprojectates possess sufficient characters to include

chapter 1 introduction to paleobotany, how fossil plants are formed

Figure 1.73 Aquilapollenites grain (Cretaceous). Bar ⫽ 10 μm. (From Jarzen, 1977.)

them within the modern flowering plant order Apiales (Farabee, 1991). Closely associated with the dating of rocks based on the presence of certain types of palynomorphs is the correlation of rock units in time and space based on the fossils within them, a discipline termed biostratigraphy (Gray et al., 1985). Various types of fossils can be found in different sedimentary environments, for example terrestrial and marine, and each may have its own biostratigraphic markers. For example, calcareous nannofossils are especially good markers in marine sediments from the Jurassic to the recent; plant spores are useful in terrestrial rocks from the Devonian onwards and diatoms (a type of microfossil) from the Paleogene to the recent. At one time, applied biostratigraphy was the method of choice in petroleum exploration. Although a number of other methods are used today, palynostratigraphic techniques are still used today to correlate strata based on the presence of certain types of microfossils. Today there are a large number of consulting companies that provide services in exploration and interpretation of petroleum and mineral deposits based on biostratigraphy and geochronology. The underpinnings of these commercial firms are based on the types and distribution of microfossils. PALEOECOLOGY

Palynology has also been extensively used as a method of characterizing past depositional systems (paleoenvironments) (Farley and Traverse, 1990). Here palynomorphs play an important role in defining, for example, the extent of a marine or terrestrial environment. In other instances, certain types of

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palynomorphs may provide valuable information about water depth, temperature, salinity, and nutrient levels where the organisms once lived. In a few cases where vertebrates and invertebrates are found with palynomorphs and plant megafossils, an even greater degree of paleoecological resolution can be obtained (Westgate and Gee, 1990). Other detailed ecological studies are possible based on the frequency and types of pollen present both geographically and stratigraphically within a confined area (Graham, 1990). The use of pollen data in association with megafossil information has had a profound influence on the interpretation of paleophytogeographic patterns throughout the world (see, e.g., Graham, 2000, 2003, on plant distribution in the Caribbean). Such studies are especially valuable when they incorporate both extant and fossil data and are founded on well-defined geographic regions of the world (Graham, 1972; 1973). Other investigations have utilized paleoecological data to show that the early flowering plants were herbs or small trees living in unstable habitats during the Cretaceous (Wing and Boucher, 1998). Certain climatic parameters can also be defined by the occurrence of certain palynomorphs, because various plants respond to minor environmental fluctuations (Pocknall, 1990). Tracing the appearance and disappearance of various palynomorphs vertically in the geologic column provides a method of tracking certain types of climatic shifts. Pollen analysis is a branch of palynology in which the relative proportions of pollen and spores are mapped vertically and horizontally; these proportions are then used to reconstruct the paleoenvironment by comparison with modern proportions of the same or closely related taxa. Although primarily applied to Quaternary deposits, similar techniques have been used in older sediments. Recovery of DNA from Holocene pollen (Bennett and Parducci, 2006) has potential for more accurate identification of certain pollen types, as well as tracking populations of plants through time. Using modern pollen and spores, Traverse (1990) determined the palynomorph load in various types of bodies of water in the Trinity River of Texas. Understanding the dynamics of a modern model system such as this is important in the interpretation of past vegetation. Pollen extracted from marine sediments, together with stable isotopes and radiolarian microfossils extracted from ocean sediment cores, were used to provide data about ocean variability on millennial timescales (Pisias et al., 2001). This information can then be used to directly compare the climate responses of continental and oceanic systems, and incorporated into broader scale climate models. Palynomorphs or microfossils are preserved from every time period of geologic history and in many types of depositional environments, so they are a valuable source

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paleobotany: the biology and evolution of fossil plants

Figure 1.74 Elaterosporites klaszii (Cretaceous). Bar ⫽ 20 μm. (From Jardiné and Magloire, 1965; courtesy M. S. Zavada.)

Figure 1.75 Elaterocolpites castelaini (Cretaceous). Bar ⫽ 20 μm. (From Jardiné and Magloire, 1965; courtesy M. S. Zavada.)

of information with which to characterize changes in paleoecosystems at different scales (Taggart and Cross, 1990). Although several books have been written on various aspects of palynology, the three-volume set, Palynology, Principles and Applications, edited by Jansonius and McGregor (1996) and the volume by Traverse (2007), Paleopalynology, provide very comprehensive and up-to-date surveys of the discipline. The recent volume edited by Van Geel (2006) focuses on the importance of various microfossils in the interpretation and reconstruction of Quaternary environments and the Glossary of Pollen and Spore Terminology (Punt et al., 2007) will be helpful in understanding the complex terminology used to described pollen and spores. Even with our current extensive knowledge of pollen and spores, some palynological preparations occasionally contain structures which cannot be identified (FIGS. 1.74, 1.75). Graham et al. (2000) described sinuous to coiled filaments similar to the elaters of Equisetum spores (Chapter 10), secondary wall thickenings of conducting elements, or germinating fungal spores. They showed that these filaments actually represent artifacts. Termed petrofilaments (FIG. 1.76), they form when hydrocarbons (asphaltenes) react with solvents in the mounting medium. Figure 1.76 Petrofilaments. Bar ⫽ 25 μm. (Courtesy A. Graham.)

ABSOLUTE DATING One of the most frequent questions asked of paleobotanists is, “How do you date fossil plants?” Most paleobotanists are familiar with the various groups of plants that lived at different points in geologic time. Consequently, when encountering

a new assemblage of plant fossils, they usually recognize the general age immediately, but this has not always been the case. Our current understanding of the age of fossil floras is based on a long series of efforts to date the various rocks

chapter 1 introduction to paleobotany, how fossil plants are formed

in which they are found. At the present time, the best absolute dating method involves the use of naturally occurring radioactive isotopes contained in various minerals that make up a rock unit. The inherently unstable radioactive isotopes undergo a series of complex transformations (decay) that lead to stable isotopes and, in the process, release energy. The rate of decay, λ, for a radioactive isotope of a given element, sometimes called the half-life, is constant (t½ ⫽ 0.693/λ). Therefore, by measuring the present amount of the radioactive isotope and the present quantity of the stable product, one can calculate how much time has elapsed since the minerals in the rock formed. For example, it is known that the long-life uranium isotope 238U decays to 206Pb with a halflife of 4.5 billion years. Consequently, by measuring the relative quantities of 238U and 206Pb in a sample, it is possible to determine the length of time the decay has been going on and thus the time of formation of the rock. A widely used technique involves the analysis of a very small amount of the relative quantities of uranium and lead contained within zircon crystals (Harrison et al., 2005). These crystals, which may be 0.1 mm in size, form as molten rock begins to cool and thus lock small amounts of uranium into their crystalline structure. This technique, which utilizes a high-resolution ion microprobe, uses a powerful beam of ions to vaporize a tiny portion (two-billionths of a gram) of a zircon crystal (Davis et al., 2003). The vapor is then passed through a mass spectrometer where the different elements are separated and analyzed. Zircon crystal geochronology has been applied widely across geologic time, including dating major earth events such as the formation of the continental crust (Harrison et al., 2005). Other radioactive isotopes differ in their half-lives, for example, 87Rb (rubidium), 48.5 billion years; 40K (potassium), 1.25 billion years; and 235U (uranium), 0.704 billion years. One difficulty in employing these dating techniques is that radioactive isotopes occur more commonly in igneous and metamorphic rocks, whereas almost all fossils occur in sedimentary deposits. Today direct isotopic dating for sedimentary rocks is possible, but only when they contain minerals that have crystallized in the environment of deposition at or near the time they were deposited. One of these is glauconite, a silicate mineral that contains potassium (Smith et al., 1998). Since the potassium consists in part of 40K, the potassium–argon method can be used. Rubidium–strontium dating of some very fine-grained sedimentary rocks also has been successful, but the procedure is difficult and not routinely applicable. A technique has been developed in which actual fossils can be dated. In the upper atmosphere, cosmic rays bombard 14N (nitrogen) isotopes to form an isotope of carbon (14C) that is radioactive. This carbon unites with oxygen to

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produce carbon dioxide (CO2). Plants take in and fix (assimilate) this carbon dioxide along with that containing the more common isotopes of carbon, 12C and 13C. Carbon dioxide is continuously assimilated during the lifetime of a plant. When the plant dies, however, it no longer exchanges carbon dioxide with the atmosphere, and thus the ratio of 14C to 13C or 12 C is fixed at that time. At that point, the 14C begins to decay to 14N with its characteristic decay rate (t½ of 14C is ⬃5730 years). For this reason, the ratio of 14C to 12C or 13C is proportional to the age of the fossil. An age limit of ⬃50,000 years (Balter, 2006) applies to this technique because of the short half-life of 14C. This technique obviously has somewhat limited usefulness in paleobotany because the bulk of the fossil plant record is far older. Human influence on the Earth has even altered the usefulness of the 14C dating method, because combustion of fossil fuels and nuclear testing have artificially altered the 14C content of the total carbon reservoir, and this has caused problems in maintaining reliable modern standard samples of carbon. Loss or addition of 14C to specimens and apparent fluctuations of past atmospheric 14C abundance also impose limitations on this dating method. Analytical techniques have been developed that allow direct detection of 14C atoms using high-energy accelerators. This method is especially important as it requires ⬍1 mg of carbon (as opposed to ⬎1000 mg in the conventional methods), and dates can be determined in a matter of hours rather than days.

GEOLOGIC TIMESCALE Frequent references will be made to the geologic timescale in succeeding chapters and a summary of geologic time is provided on the inside front and back cover of this volume. In many ways, the naming of rock units is similar to the naming of organisms, in that the geologic timescale is not fixed, but is constantly updated and refined by the International Commission on Stratigraphy (ICS), part of the International Union of Geological Sciences (IUGS). At the formation level, there is a type section of that formation, where rocks that are typical for that formation are exposed. Periods are formally defined at the base of each period by a Global Stratotype Section and Point (GSSP); the GSSP is designated on the ICS timescale as a golden spike. The global stratotype section for the base of a period is somewhere in the world where an excellent section of rocks is exposed and is agreed upon by a committee of experts. For more information, please refer to Gradstein et al. (2004) or the ICS web page, www.stratigraphy.org. There are two types of units in geologic time: rock units and time units. Rock (lithostratigraphic) units refer to the

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paleobotany: the biology and evolution of fossil plants

physical rocks themselves and the terms, Lower, Middle, and Upper are used for these, for example this fossil was found in Lower Devonian rocks. Time (chronostratigraphic) units refer to the period of time represented by those rocks, and use time units (i.e., Early, Middle, and Late), for example, plants of the Early Devonian. Throughout this book, you will see the following abbreviations for geologic time: ka, Ma, Ga—These stand for, respectively, thousands of years, millions of years, and billions of years (gigayears) before present. These are used for dates, for example this plant lived 450 Ma (450 million years ago). kyr, myr, byr (sometimes written Gyr)—These stand for intervals of time, for example this group survived for 20 myr.

BIOLOGICAL CORRELATION Because radiometric dates are not available for all sequences of rocks in specific geographic regions, it becomes necessary to position a given rock unit accurately relative to its absolute age, a type of relative dating. One way in which a sequence of sedimentary rocks can be grouped according to age is through the use of index fossils. To be effective, an index fossil should (1) distinguishable from other fossils and easily identifiable, (2) have existed during a relatively short period of geologic time, (3) be abundant, (4) be widely distributed geographically, and (5) have lived in different environments, so that it may be preserved in different types of sedimentary rocks. Obviously, not many fossils fulfill all these requirements, and assemblages of several fossil taxa (assemblage zone) are typically more useful than a single species. Generally, the most useful organisms for correlation from one section of rocks to another are those that lived in ancient seas. Pelagic organisms (those that live in the open sea and not on the bottom) provide the best long-range correlations because of their worldwide distribution, at least within certain climatic zones. These organisms include such planktonic forms as diatoms (Chapter 4), foraminifera, silicoflagellates, and coccoliths (FIG. 4.43). These organisms are especially important because their skeletal remains are so small that a large number can be concentrated in a small sample, such as the cuttings obtained from a well boring. Other organisms, such as those that inhabited the ocean floors (benthic forms), typically have a spatially restricted distribution that enables them to be used effectively in correlations of a more local extent. In terrestrial rocks, some of the best index fossils are pollen grains and spores (Gonzalez et al., 2006; Souza, 2006).

They can be carried long distances by wind and, consequently, can be deposited in a wide variety of sedimentary environments. Palynostratigraphy has been an especially important tool in providing correlation between marine and non-marine rocks and in determining the various ecological conditions under which plants lived (Dimitrova et al., 2005). Plant megafossils have also been useful in biostratigraphy, especially when used in the form of assemblage zones. Such studies extend from some of the earliest land plants (Edwards and Richardson, 2004) to measuring Holocene vegetational changes. Noteworthy among plant megafossils used as index fossils are a variety of Carboniferous foliage types (see Chapter 16), which have proven useful in establishing stratigraphic sequences in certain geographic regions (Diaz, 1983, 1985). For example, late Paleozoic foliage types have been useful in delimiting biostratigraphic zones in North America (Read and Mamay, 1964; Gillespie and Pfefferkorn, 1979), southwestern Germany (Germer, 1971), and northern France (Laveine, 1987). In some cases, megafossils have been more reliable than palynology, as palynomorphs are often difficult to extract from the high-rank coals that comprise some of the stratotype sections. In other instances, the identification of particular taxa has been useful in precisely dating tectonic events, such as the Upper Carboniferous folding phases in northwestern Spain (Wagner, 1966), and in documenting climatic changes (Wagner, 2004). There can be little doubt that as fossil plants are better understood they will become increasingly important as stratigraphic markers in biozonation and correlation.

SYSTEMATICS AND CLASSIFICATION This book emphasizes the origin, evolution, and diversity of the major groups of plants based on the fossil record, and their relationships through geologic time; floristic changes through time are discussed to a lesser extent. To do this, we need to address the systematics of plants. The field of systematics is concerned with classifying, naming, and determining the evolutionary relationships of taxa. Taxon (pl. taxa) is a general name to indicate any level of organization (i.e., a species, a genus, a family, etc.). Within systematics, taxonomy is the process of describing and classifying organisms into natural groups and nomenclature is the process of naming taxa. In this book, we will use Linnean nomenclature, in which each plant has a two-part name, sometimes called a binomial, which consists of a genus name and a species name (specific epithet). The rules of naming plants are complex and are encoded in the International Code of Botanical Nomenclature (ICBN) (McNeill et al., 2006), which is refined every 4 years.

chapter 1 introduction to paleobotany, how fossil plants are formed

In spite of long study and continued refinements, naming plants still represents a highly subjective exercise. Generally, all classification systems are based on the same type of evidence: shared features. Shared features allow one to recognize genera, families, and other higher categories of a classification scheme (Funk and Brooks, 1990). Such features may fall into two general categories. In one group are the primitive features (plesiomorphies) that evolved relatively early in the evolution of a group of organisms, such as the vascular tissue present in most terrestrial plants. Features of this type may be regarded as evolutionary holdovers that have persisted, but tell us little about the relationships among members of the group, because every member of the group has the same feature. The other group of characters is believed to have evolved more recently. These advanced or specialized features (apomorphies) can be used to identify organisms that have a common ancestry. The cladistic or phylogenetic system of systematics has the goal to produce a hierarchical organization of taxa based on shared, derived features (synapomorphies) that reflect the evolution of particular groups of organisms (Duncan and Stuessy, 1984). Classifications that group organisms based on the overall similarity of characters, whether both primitive or derived, are termed phenetic systems. Another system that has been proposed for classifying living organisms, including plants, is the Phylocode (Cantino and de Queiroz, 2006). This system is very controversial, but is meant to reflect phylogenetic systematics more than Linnean taxonomy (Nixon et al., 2003). Monophyletic groups, that is those consisting of a single common ancestor and all descendants of that ancestor (clade), are defined solely by their position on the tree of life. Clades may have any rank, but the rank is added after nomenclature is completed. It will be interesting to see if this system gains recognition within the plant systematic community since many plant taxa are now thought to be paraphyletic (Rieseberg and Brouillet, 1994); paraphyletic groups include the ancestor and some, but not all, of its descendants). It would appear reasonable to assume that a classification scheme like the Phylocode, which includes only taxa that fit into monophyletic groups, will not be an accurate and useful tool for arranging the enormous biological diversity represented in the fossil record (Briggs and Crowther, 2001). Moreover, it is difficult to envision how fossils would be treated in the phylogenetic nomenclature of this classification system.

the plants are represented in the fossil record as disarticulated parts. This has resulted in the establishment of a special system of nomenclature for parts of fossil plants. As in other areas of botany, fossil plants are named according to the rules in the ICBN, but in paleobotany each disarticulated part is given a separate generic and specific name. In the past, paleobotanists had two types of names for parts of fossil plants. An organ genus was designated when there was enough information to assign a plant part to a family. For example, Lepidodendron, Stigmaria, and Lepidostrobus (Brack-Hanes and Thomas, 1983) (FIG. 1.77) are generic names used to designate parts (stem, roots, and cones) belonging to a particular type of Carboniferous lycopsid. The form genus was used for fossil plant parts that could not be assigned to a family, for example a piece of wood that could be assigned to the gymnosperms, but not to any particular group of gymnosperms. Originally, an organ genus was considered to represent a more natural (i.e., phylogenetic) taxon than a form genus, but confusion arose because names have been given to the same plant parts in different states of preservation or development. Today, the term morphotaxon has replaced the designations form and organ genera in paleobotany. A morphotaxon is a fossil taxon which, for nomenclatural purposes, comprises only the parts, life history stages, or preservational states represented by the corresponding nomenclatural type (Chaloner, 2004). The nomenclatural type is the plant fossil on which the name is based. Why do paleobotanists give names to different parts of the same plant? The first reason for naming parts is so that the fossils can be studied and referred to in publications

NOMENCLATURE OF FOSSIL PLANTS

Historically, paleobotanists have utilized a somewhat artificial classification system, since in almost all instances

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Figure 1.77 Sheila Hanes.

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paleobotany: the biology and evolution of fossil plants

and discussed with other paleobotanists. The other reason is that some identical plant parts may be attached to different plants, for example the Carboniferous lycopsid rooting organ Stigmaria, a morphogenus, has been found attached to different genera of stems. In a case like this, the name of the part is maintained, even though the entire plant has subsequently been reconstructed. The name is also maintained because fossil Stigmaria is still found unattached, and a name is necessary to describe and study the part. In addition, some fossil plant parts, despite extraordinary preservation, cannot be distinguished as belonging to only one group of plants. For example, some species of the Carboniferous foliage type Sphenopteris were borne by marattialean ferns (Chapter 11), and other species of this morphotaxon were produced by lyginopteridalean seed ferns (Chapter 16). Since most plants are constructed of many parts, referring to the entire plant once it has been reconstructed requires a complex system of nomenclature. In general, three procedures are followed when the entire plant is reconstructed: (1) the entire organism is provided with a new name, (2) the whole organism bears the generic name of the part that has priority, that is the first part given a formal name, or (3) the whole plant is referred to informally, for example the “Lepidodendron” plant. Non-paleobotanists may find the nomenclature used in paleobotany confusing and perhaps cumbersome, but the way that fossil plants are preserved necessitates its use, and it is currently the only system that provides for an orderly arrangement of names and, most importantly, for the retrieval of information on plant parts. Some have suggested that the Linnaean system of nomenclature be abandoned for certain types of fossils, especially the use of names that suggest affinities with extant taxa when the exact affinities are unknown (Spicer, 1986, for Cretaceous and Cenozoic angiosperm leaves). Hughes (1989) championed a system in which pollen and other plant parts were given artificial names, so-called paleotaxa (Chapman and Smellie, 1992 for fossil wood), but the system has never been in wide use among paleobotanists. CLASSIFICATION OF ORGANISMS

Each author has his or her own ideas concerning the way organisms should be organized, or in the case of plants, whether they represent a single kingdom or multiple kingdoms. With this in mind, the classification scheme in Appendix 1 is presented merely as a guide to the groups of

algae, fungi, bryophytes, and vascular plants that are discussed in this book. In the case of some groups, such as the hyperdiverse flowering plants, there are so many families with a meager fossil record, or no fossil record at all, that it would be impossible to include them all, so we have tried to provide a sampling of major groups and interesting examples. For the angiosperms, we have followed the system in Cronquist (1988) for the most part, with attention to the system of the Angiosperm Phylogeny Group (1998, 2003); for the algae (Chapter 4), the system in Lee (1999), for the hornworts and bryophytes (Chapter 5), the system in Frahm (2001a), and for the fungi (Chapter 3), The Mycota, Volumes VIIA and VIIB (McLaughlin et al., 2001a, 2001b). Some readers may wish to adapt the plant groups presented in the following chapters to a system with which they feel more comfortable.

BACKGROUND READING There are many approaches that one might take in the preparation of a volume dealing with fossil plants. Through the years there have been many excellent books on paleobotany that have covered the discipline from many perspectives. We have included a number of these in the bibliography so that the reader may obtain additional information on some of the plant groups presented here, or additional ones not discussed. The following volumes (and references cited therein) will provide supplemental details on many fossil plants: Hirmer, 1927; Arnold, 1947; Darrah, 1960 (FIG. 1.50); Andrews, 1961; Delevoryas, 1962; Mägdefrau, 1968; Archangelsky, 1970; Banks, 1970; Emberger, 1968; Beck, 1976a, 1988; Hughes, 1976 (FIG. 22.15); Remy and Remy, 1977; Taylor, 1981; Thomas, 1981a; Stewart, 1983 (FIG. 14.116); Gensel and Andrews, 1984; Tiffney, 1985; Spicer and Thomas, 1986; Meyen, 1987; Thomas and Spicer, 1987; Friis et al., 1987; Taylor and Taylor, 1993; Kenrick and Crane, 1997a; Stewart and Rothwell, 1993; Jones and Rowe, 1999 (for methods in paleobotany and palynology); Gensel and Edwards, 2001; Willis and McElwain, 2002; Anderson and Anderson, 2003; Kenrick and Davis, 2004; Anderson et al., 2007; and the Traité de Paléobotanique series, published under the direction of E. Boureau (FIG. 10.108) (Boureau, 1964; Boureau et al., 1967; Andrews et al., 1970; Boureau and Doubinger, 1975) (FIG. 15.14).