(Open Access) Three-dimensional visualization of fossil flowers, fruits, seeds, and other plant remains using synchrotron radiation X-ray tomographic microscopy (SRXTM): new insights into Cretaceous plant diversity (2014) | Else Marie Friis

Q: What future works have the authors mentioned in the paper "Three-dimensional visualization of fossil flowers, fruits, seeds, and other plant remains using synchrotron radiation x-ray tomographic microscopy (srxtm): new insights into cretaceous plant diversity" ?

SRXTM has already been informative where it has been deployed in paleobotany, but the full possibilities of these techniques are still relatively underexplored. The combination of SRXTM with the availability of a large numbers of diverse and well-preserved specimens offers the possibility of a new phase of rapid progress in their understanding of Cretaceous and other fossil plants. In many cases, the critical details revealed by the application of SRXTM have created opportunities to compare the fine structure of fossils with those of extant taxa, raising the possibility of also using SRXTM to study complex 3-D structures in living plants. This kind of material requires higher energies, and particularly for larger specimens where lateral merging and vertical stacking is required the acquisition time may be extensive.

Three-dimensional visualization of fossil flowers, fruits,

seeds, and other plant remains using synchrotron

radiation X-ray tomographic microscopy (SRXTM): new

insights into Cretaceous plant diversity

Authors: Friis, Else Marie, Marone, Federica, Pedersen, Kaj

Raunsgaard, Crane, Peter R., and Stampanoni, Marco

Source: Journal of Paleontology, 88(4) : 684-701

Published By: The Paleontological Society

URL: https://doi.org/10.1666/13-099

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THREE-DIMENSIONAL VISUALIZATION OF FOSSI L FLOWERS, FRUITS,

SEEDS, AND OTHER PLANT REMAINS USING SYNCHROTRON RADIATION

X-RAY TOMOGRAPHIC MICROSCOPY (SRXTM): NEW INSIGHTS INTO

CRETACEOUS PLANT DIVERSITY

ELSE MARIE FRIIS,

FEDERICA MARONE,

KAJ RAUNSGAARD PEDERSEN,

PETER R. CRANE,

AND MARCO STAMPANONI

2,5

Department of Palaeobiology, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden, ,else.marie.friis@nrm.se.;

Swiss Light Source, Paul Scherrer Institute, CH-5232 Villigen PSI, Switzerland, ,federica.marone@psi.ch.; ,marco.stampanoni@psi.ch.;

Department of Geology, University of Aarhus, DK-8000 Aarhus, Denmark, ,krp@geo.au.dk. ;

Yale School of Forestry and Environmental Studies

195 Prospect Street, New Haven, CT 06511, USA, ,peter.crane@yale.edu.; and

Institute for Biomedical Engineering, ETZ F 85,

Swiss Federal Institute of Technology Zu¨rich, Gloriastrasse 35, 8092 Zu¨rich, ,stampanoni@biomed.ee.ethz.ch.

ABSTRACT—The application of synchrotron radiation X-ray tomographic microscopy (SRXTM) to the study of mesofossils

of Cretaceous age has created new possibilities for the three-dimensional visualization and analysis of the external and

internal structure of critical plant fossil material. SRXTM provides cellular and subcellular resolution of comparable or

higher quality to that obtained from permineralized material using thin sections or the peel technique. SRXTM also has the

advantage of being non-destructive and results in the rapid acquisition of large quantities of data in digital form. SRXTM

thus refocuses the effort of the investigator from physical preparation to the digital post-processing of X-ray tomographic

data, which allows great flexibility in the reconstruction, visualization, and analysis of the internal and external structure of

fossil material in multiple planes and in two or three dimensions. A review of recent applications in paleobotany

demonstrates that SRXTM will dramatically expand the level of information available for diverse fossil plants. Future

refinement of SRXTM approaches that further increases resolution and eases digital post-processing, will transform the

study of mesofossils and create new possibilities for advancing paleobotanical knowledge. We illustrate these points using

a variety of Cretaceous mesofossils, highlighting in particular those cases where SRXTM has been essential for resolving

critical structural details that have enhanced systematic understanding and improved phylogenetic interpretations.

INTRODUCTION

HE PAST thirty to forty years have seen significant a dvances

in understanding patterns of str uctural diversification

during the early phases of angiosperm evolution. Central i n

these developments has been the discovery in Cretaceous

sediments of small 3-D ve getative and reproductive struc tures

(mesofossils), including angiosperm flowers, fruits, and seeds

(Tiffney, 1977; Friis and Skarby, 1981; see also referenc es in

Friis et al., 2011) . The se f ossils, which are preserved both as

lignitized specimens and as charcoal, often have e xquisite

preservation of complex form as well as superb preservation of

cellular and other internal details. Initially, this material was

studied with considerable success using scanning electron

microscopy (SEM), occasionally supplemented by conventional

serial sectioning after embedding the specimens in p lastic. Ove r

time technical advances in SEM also improved resolution in the

routine microscopy of surface features.

More recently, the application of synchrotro n radiat io n X-ray

tomographic microscopy (SRXT M) has provided a new way of

studying diverse mesofossils through the digita l capture of high-

resolution, large, X-ray tomographic, datasets. Unlike with

conventional sectioning, these datasets are created withou t

damage to the specimen, and they enable the rec onstruction,

visualization, and analysis of the internal and external structure

of critical fossil material with new flexibility. Two-dimensional

sections can be constr ucted in multiple orientations, 3-D

reconstructions can be created and manipulated, and complex

specimens, such as flowers, can be dissected digitally rather

than physically. S RXTM gre atly e nhances the information that

can be o btained from fossil plants for comparative and

phylogenetic studies (Friis et al., 20 07).

Extensive datasets on fossil plants have been accumulated

from SRXTM analyses at the Tomcat beamline (Stampanoni et

al., 2006) a t the Swiss Light Source (SLS) covering material

from the Carboniferous (Scott et al., 2009), Permian (Slater et

al., 2011), Cretac eous (Friis et al., 2007; von Balthazar et al.,

2007; von Balthazar et al., 2008; Friis et al., 2009b; Friis et al.,

2010; Friis and Pedersen , 2011; He

rmanova

et al., 2011; von

Balthazar et al., 2011; Friis and Pedersen, 2012; Friis et al.,

2013a; Friis e t al., 2013b; Friis et al., 2014a, 2014b; Mendes et

al., 2014), and Cenozoic (Smith et a l. , 2009a; Smith et al.,

2009b; Collinson et al., 2013 a; Collinson et al., 2013b). The

only other published studies on Cretace ous flowers examined at

other beamlines is that of Glandulocalyx upatoiensis Scho

nen-

berger et al., 2012, analyzed mainly at th e b eamline 2-BM of the

Advanced Ph oton Source at the U.S. Department of Energy

Argonne National Laboratory, but also at the BL20B2 beamline

of the Super Proton ring-8 GeV (SPr ing-8) at the Japan

Synchrotron Radiation Research Institute (Scho

nenberger et

al., 2012), and unnamed flower studied at the beamlines BM05,

ID19, and ID22 at ESRF, Grenoble (Mor eau et al., 2014). There

are also now several studies of extant floral structur es using

laboratory based X-ray CT (e.g., Staedler et al., 2013).

In this paper we prov ide an overview of the SRXTM

techniques applied so far to understand and visualize the

detailed structure of Cretaceous fossil flowers and other plant

mesofossils. We focus on examples from the very substantial

datasets collected a t the SLS and highlight those cases where

SRXTM has resolved critical structural details that have

684

Journal of Paleontology, 88(4), 2014, p. 684–701

0022-3360/14/0088-684$03.00

DOI: 10.1666/13-099

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improved systematic und erstanding and phylogenetic interpre-

tation.

FOSSIL MATERIAL

The first substantia l discovery of a Cre taceo us mesofossil

assemblage c ontaining well-preserved flowers w as from fluvi-

atile-lacustrine sediments of late Santonian to early Campanian

age at the

Asen locality, Southern Sweden (Friis and Skarby,

1981). Since the n many similar floras have been disc overed and

studied from localities of Creta ceous age in Europe, North

America, Central and East Asia, Antarctic a, and New Zealand

(for referenc es se e Friis et al., 2011). The Cretaceous

mesofossils occur as iso lated organs in unconsolidated clays

and sands, and are extracted by sieving in water. Intermediate in

size between the larger fossils (macrofossils) that have typically

been the focus of Cr etaceous paleobotanical re search, and fossil

pollen and spores (microfossils), the flowers, fruits, seeds an d

other fossils that comprise mesofossil assembla ges rare ly exc eed

more than a few millimeters in length.

Fossil assemblages containing isolated plant fra gments are

common in Cenozoic strata (e.g, Reid and Reid, 1915; Chandler,

1957; Kirchheime r, 195 7; Dorof eev , 1963; Friis, 1985; see also

references in Mai, 1995), and have also bee n obtained from

older sediments (Edwards, 1996; Crane and Herendeen, 2009),

but sever al features of many Cretaceous mesofossil a ssemblages

are unusual. In particular, the small size of the individ ual fossils,

and the presence of large numbers of tiny fossil f lowers, often

with delicate petals, s tamens and other floral parts preserved,

was completely unanticipated. Also unusual is the abundance of

charcoal in these Cretaceous mesofossil assemblages. Compa-

rable assemb lages of Cenozoic age, prepared using the same

techniques, typically contain fossils with a much wider range of

sizes (Tiffney, 1984; Eriksson et al., 2000a), are usually

preserved as lignite rather than cha rcoal, and rarely contain

fossil flowers (Friis et al., 2011).

The abundance of charcoal in Cretac eous mesofossil assem-

blages indicates t hat na tural fires were a major fea ture of

Cretaceous landscapes (Friis et al., 2011; Brown et al., 2012). In

the process of c harcoalif ication , the incomplete combustion of

plant ma teria l under conditions of reduced oxygen resulted in

excellent preservation of the 3-D form and cellular detail of

diverse plant parts. While some shrinkage of the original plant

material often occurs during charc oalification (Harris, 1981;

Lupia, 1995), and cell walls are typically homogenize d, the

shape of the cells is gener ally more or le ss unaltere d (Scott and

Jones, 1991), and very delicate structural details are fre quently

preserved, as illustrated in the descriptive part of this revie w.

The 3-D preservation of exquisite cellular details, combined

with their small size, makes ma ny fossil flowe rs and other

reproductive structures from Cretaceous me sofossil floras

especially well-suite d for SRXTM. The application of the new

technique to charcoalified material has allowed mesofossils to

be examined with an unprecedented level of detail and is

advancing our unde rstanding of Cretaceous plant diversity in

substantial ways.

SRXTM TECHNIQUES

Synchrotron radiation har d X-ray tomographic microscopy

(SRXTM) represents a great advance over the application of

conventional X-ray approaches in paleontology and has proved

a powerf ul technique for the non -destructive investigation of

internal structure in a variety of optically opaque samples.

Broadly similar SRXTM tec hniques c an b e ap plied to a wide

range of paleobiological ma teria l, but here we focu s on the

techniques used so far f or the study of plant mesofossils.

Preparation of plant mesofossils for SRXTM is straightfor-

ward. Specimens are analyzed non-destructively and are n ot

altered physica lly by the process. Unlike SEM no coating is

required, and unlike with c onventi onal sec tioni ng of livi ng

material dehydrating, f ixing or staining of the specimen is not

needed. The specimen is usually attached to a support (e.g., a

brass pin or SEM stub) with a diameter compatible with that of

the beamline sample hold er (Fig. 1). Attachment of the

specimen to the support i s usually done with nail polish for

lighter, coalified mesofossils or with wax for heavier, permin-

eralized specimens. Other adhesive typically used for attaching

specimens to SEM stubs can also be used. Removal of

specimens attached with nail polish can be done easily with a

thin blade of a knife, particularly if the contact to the adhesive is

small.

The specimens are usually studied also by SEM either prior to

or after SXRTM. No additional sample preparation is necessary

for investigation of specimens that have previously been coated

with gold/platinum and analyzed with SEM. The coating does

not obscure internal features. Remounting of spe cimens from

SEM stubs may facilitate reconstruction, but is not a

requirement sinc e re-orientation of spec imens that have be en

mounted obliquely can be achieved physically using a

goniometer (Mader et al., 2011) or digitally using the

reconstruction software (Fig. 2).

Initial examina tion uses 2-D r adiographs taken for different

sample orientations using a parallel beam. Photons transmitted

through the sample are converted to visible light by a scintillator

screen. The image can then be magnified using light microscope

optics before being recorded by a digital camera (Fig. 2.1, 2.2).

Data from 2-D radiographs provide useful but cumulative

FIGURE 1—Close-up view of the TOMCAT end station showing the sample

holder with a fossil flower mounted on a brass stub, 3 mm in diameter, in front

of the microscope. (Paul Scherrer Institute photo).

FRIIS ET AL.—3-D VISUALIZATION OF PLANTS USING SRXTM 685

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information on the internal structure of the specimen along the

beam path. However, it is not possible to determine from 2-D

projections if a specific fe ature is loca ted at the front or back of

the specimen. To access such 3-D information, a second step

requires combining the recor ded radiographic dataset (reo rdered

into sinograms) using algorithms ba sed on Fourier analysis (e.g.,

filtered back-projection) or iterative methods.

SRXTM takes advantage of the absorption and refraction of

X-rays during their i ntera ct ion with matter resulting in different

imaging modalities. In absorption contrast tom ographic m icros-

copy, X-rays are selectively a ttenuated as they traverse the

sample according to the Bee r-Lambe rt law:

I ðZ; EÞ¼I

ðEÞexp



ðZ; EÞdz



;

where I(Z,E)andI

(E) are the X-ray beam intensity after and

before the specimen. The linear attenuation coefficient l

(Z,E)

strongly depend s on the atomic number Z: this provides high

contrast between materials with different densities, if the X -ray

beam energy E is properly selected.

When the ana lyzed sample is made of light elements, or

elements with a similar atomic number Z, contrast i s i nstead

obtained by exploiting the refractionoftheX-raybeamat

material boundaries in the study object and the resulting

interference phenomena. The refraction angles are small, but

can be determined with great accuracy using phase contrast

techniques. T he methods c ommonly deployed in paleontology

use the free-spac e propagation approach (Snigirev et al., 1995;

Cloetens et al., 1996). The main adva ntages with respect to

other existing approaches, such as interferometry (Bonse an d

Hart, 1965; Weitkamp et al., 2005) and analyz er syste ms (Davis

et al., 1995; Chapman et al., 1997) are the high spatial resolution

and uncomplicated setup that d oes not require additiona l

hardware. In the simplest case, pure, so-called, edge-enhance-

ment is exploited by increasing the distance between the sample

and the detector. Fresnel fringes are localized at domain

boundaries and arise from th e interference of the refracted and

the directly transmitted beam in case of spatially (partially)

coherent r adiation. This permits clear visualization of internal

boundaries, although the actual contrast between regions with

different composition is not improved compared to standar d

absorption contr ast tomography. This technique is routinely

used for understanding the internal struc tu re of fossil flowers,

fruits, seeds, and other mesofossils.

FIGURE 2—SRXTM images of holotype of Silvianthemum suecicum (S100376) from the Late Cretaceous

Asen locality, Sweden; dataset acquired using a 103

objective and 20 lm thick LAG:Ce scintillator (voxel size 0.74) at 10 keV; specimen charcoalified and mounted obliquely on SEM stub. 1, 2, 2-D dark and flat

field corrected radiographic projections for two different sample orientations; 3, 2-D orthoslice of flower bud in longitudinal view through one style, sample not

re-oriented; 4, 5, 3-D surface rendering showing external morphology of flower bud in apical and lateral views, respectively; 6, electronically re-oriented

longitudinal section through center of flower bud in 3-D cut voltex (transparent rendering between orthoslices 740–780). Scale bars¼500 lm.

686 JOURNAL OF PALEONTOLOGY, V. 88, NO. 4, 2014

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More advanced approaches enable the extra ction of (phase)

information coded in the observed Fresnel fringes to further

boost the contrast between domains that have similar compo-

sitions. The simplest algorithms for phase retrieval (Bronnikov,

2002; Paganin et al., 2002; Groso et al., 2006) work with data

acquired at one single sa mple-de tector distance . In this case the

setup and protocol is the same a s for standard absorption based

experiments. These technique s are not fully quantitative and

rely on different assumptions, whic h ca n often be partially

relaxed, but the incre ased contrast is generally helpful in

particularly low absorbing specimens. The concomitant reduc-

tion in spatial resolution, which is sometimes observed, can be

mitigated by including the high frequenc y component of the

original data.

Fully quantitative, high resolution results (holotomography;

Cloetens et al., 1999) can be obtained using datasets a cquired at

multiple sample-detector distances. Holotomography is, how-

ever, rarely use d bec ause of the m ore complicated setup, slower

data acquisition and more complex data post-processing tha t is

required.

RECENT DEVELOPMENTS IN SRXTM TECHNIQUES

Spatial resolution.—For parallel beam geometry, the available

field of view is determined by the optical configuration chosen

and the resolution that is required. In general, the large field of

view necessary to accommodate a sample of large volume results

in a low magnification dataset whereas higher resolution can be

achieved if the field of view is more restricted. For instance, a

203 objective coupled to a sCMOS (scientific complementary

metal-oxide-semiconductor) detector provides a pixel size of

0.375 lm across a field of view of 0.8530.7 mm

, which is often

insufficient for the complete observation of larger specimens at

this resolution. When expansion of the available field of view in

the direction parallel to the rotation axis is desirable, but high

resolution is still required, a stack of several independent

tomographic scans can be acquired. However, an increase of

the field of view in the direction perpendicular to the rotation axis

cannot be obtained by simply juxtaposing single tomographic

datasets in this way. Instead it is necessary to merge projections

covering the desired field of view laterally prior to tomographic

reconstruction.

Although a multi-fold lateral expansion is technically feasible

(Haberthu¨r et al., 2010), for most of the mesofossil material

examined so far at the SLS a two-fold extension is often

sufficient. In such cases, prior to the scan, the rotation axis is

positioned at either side of the field of view, rather than in the

center, though still ensuring a small overlap for 1808 opposed

projections. Then, equiangular distributed projections over 3608

are acquired. The total number of projections is also increased

compared to standard tomographic scans, so as to still satisfy the

sampling theorem. Subsequently, projections acquired at an angle

h8 and h8þ1808 need to be merged, for instance using the

overlapping region and a cross-correlation technique, if the exact

position of the rotation axis is not known a priori. A single

tomographic volume can then be obtained using the merged

projections and a standard reconstruction algorithm.

In studies performed so far, high resolution imaging of small

fossil flowers with a diameter smaller than 0.7 mm has mostly

been accomplished using a 203 objective and a 20 lm thick

LAG:Ce (Cerium doped Lutetium Aluminum Garnet) scintillator

screen. Specimens as small as 0.3–0.4 mm, as is the case for

instance for megaspores, would entirely fit in the field of a 403

objective and could potentially be resolved even more finely

providing that the experimental setup is optimized for this

purpose. If higher magnification microsc ope objectives are

coupled to thinner scintillator screens, spatial resolution can be

pushed to the sub-micron regime even for experimental setups in

parallel beam geometry as is shown here for the Cretaceous

megaspore Arcellites (Fig. 3). The improvement in resolution

provided by this configuration is evident (Fig. 3.3). The 2-D slice

(Fig. 3.1) was extracted from a tomographic dataset acquired

using a 203 objective coupled to a 20 lm thick LAG:Ce

scintillator. Comparison with the slices (Fig. 3.2, 3.3) originating

from a tomographic volume obtained with a 403 objective and a

5.9 lm thick LSO:Tb (Terbium doped Lutetium Oxyorthosilicate,

SiO

) scintillator screen shows clearly the details of the

megaspore wall structure, including an outer layer penetrated by

narrow, straight canals about 0.4 lm in diameter and 7 lm long.

Three-dimensional reconstructions show the spatial distribution

of the canals (Fig. 3.4–3.6). Based on these results a new species

of Arcellites will be established and a detailed description of

megaspore morphology and wall structure presented (Friis et al.,

2014b). Ongoing optimization of the setup used for the initial

acquisition of the data (Fig. 3.2, 3.3) includes improvement of the

scintillator screen positioning system, ensuring homogeneous

focus across the entire field of view, and a pre-processing

alignment step to correct for any possible mechanical vibrations

or imperfections in the rotation that would lower resolution.

Density resolution.—During the past few years, microtomo-

graphy end-stations at third generation synchrotron sources have

been optimized in important ways resulting in datasets of

astonishing quality. In early applications of SRXTM to coalified

Cretaceous mesofossils, phase retrieval approaches were often

necessary to achieve the desired resolution (Friis et al., 2007).

However, now, simple absorption contrast is often sufficient.

New developments in detector technology (e.g., sCMOS), as well

as improvements in scintillating materials, have significantly

improved the signal-to-noise ratio in tomographic datasets and

resulted in improved density resolution. These developments have

also enhanced the efficiency of the tomography setup, reducing

the time necessary for the acquisition of a high-resolution scan by

approximately a factor of 20. This improvement in efficiency

enables the acquisition protocol to be optimized (e.g., increased

number of projections, frame-averaging) to boost signal-to-noise

ratio and ultimately density resolution. When applied to these

highest quality tomographic datasets, new phase retrieval

algorithms permit density resolution to be pushed even further.

Efficient data acquisition and increased computing power also

allows the complementarity of absorption and phase contrast

tomographic microscopy (spatial resolving power vs. density

resolving power) to be easily exploited. A single specimen can be

readily examined using both absorption and phase contrast

tomographic microscopy. For small, low absorbing samples (1

mm in diameter or smaller), such as many Cretaceous flowers, it

is generally sufficient to acquire one tomographic dataset with the

object positioned as close to the microscope as mechanically

allowed by the setup (typically at least 5 mm). From these data

two different tomographic volumes can be reconstructed.

Projections can be reconstructed using algorithms for absorp-

tion-based tomography providing the 3-D distribution of the X-

ray linear attenuation coefficient with edge-enhancement. Despite

little contrast due to the small difference in the linear attenuation

coefficient between air and the specimen, datasets reconstructed

in this way are characterized by high resolution and sharp edges.

Alternatively, information coded in the Fresnel fringes in the

same projections can be unraveled by phase retrieval approaches

prior to tomographic reconstruction to yield the 3-D distribution

of the pseudo-phase information (compare Fig. 3.2, 3.3). In this

case the results are generally not truly quantitative, and phase

contrast tomographic volumes often have lower resolution, but

the boosted contrast is useful to differentiate among domains with

similar compositions. Both approaches have inherent

FRIIS ET AL.—3-D VISUALIZATION OF PLANTS USING SRXTM 687

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Three-dimensional visualization of fossil flowers, fruits, seeds, and other plant remains using synchrotron radiation X-ray tomographic microscopy (SRXTM): new insights into Cretaceous plant diversity

Figures

Citations

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References

Early angiosperm diversification : The diversity of pollen associated with angiosperm reproductive structures in early Cretaceous floras from Portugal

Seed Size, Fruit Size, and Dispersal Systems in Angiosperms from the Early Cretaceous to the Late Tertiary.

Theory of quantitative phase-contrast computed tomography.

Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales

Implementation of a fast method for high resolution phase contrast tomography

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Early Flowers and Angiosperm Evolution

Trends in synchrotron-based tomographic imaging: the SLS experience

Monetianthus mirus gen. et sp. nov., a Nymphaealean Flower from the Early Cretaceous of Portugal

Early Cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales-Erdtmanithecales-Gnetales group

Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales

Frequently Asked Questions (2)

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