New evidence of the reproductive organs of Glossopteris based on

J Plant Res (2014) 127:233–240
DOI 10.1007/s10265-013-0601-3
JPR SYMPOSIUM
Palaeobotany:Old but new stories on plant diversity
New evidence of the reproductive organs of Glossopteris based
on permineralized fossils from Queensland, Australia. II:
pollen-bearing organ Ediea gen. nov
Harufumi Nishida • Kathleen B. Pigg
Kensuke Kudo • John F. Rigby
•
Received: 10 August 2013 / Accepted: 29 September 2013 / Published online: 29 October 2013
Ó The Botanical Society of Japan and Springer Japan 2013
Abstract Ediea homevalensis H. Nishida, Kudo, Pigg &
Rigby gen. et sp. nov. is proposed for permineralized
pollen-bearing structures from the Late Permian Homevale
Station locality of the Bowen Basin, Queensland, Australia.
The taxon represents unisexual fertile shoots bearing helically arranged leaves on a central axis. The more apical
leaves are fertile microsporophylls bearing a pair of multibranched stalks on their adaxial surfaces that each supports
a cluster of terminally borne pollen sacs. Proximal to the
fertile leaves there are several rows of sterile scale-like
leaves. The pollen sacs (microsporangia) have thickened
and dark, striate walls that are typical of the Arberiella type
found in most pollen organs presumed to be of glossopterid
affinity. An examination of pollen organs at several
developmental stages, including those containing in situ
pollen of the Protohaploxypinus type, provides the basis for
a detailed analysis of these types of structures, which bear
H. Nishida (&)
Faculty of Science and Engineering, Department of Biological
Sciences, Chuo University, 1-13-27 Kasuga, Bunkyo-ku,
Tokyo 112-8551, Japan
e-mail: [email protected]
H. Nishida
Graduate School of Science, University of Tokyo, Tokyo, Japan
K. B. Pigg
School of Life Sciences, Arizona State University, Box 874501,
Tempe, AZ 85287-4501, USA
K. Kudo
4-17-1 Kitakokubunjidai, Ichihara, Chiba 290-0013, Japan
J. F. Rigby
School of Earth, Environment and Biological Sciences,
Queensland University of Technology, Brisbane,
QLD 4001, Australia
similarities to both compression/impression Eretmoniatype glossopterid microsporangiate organs and permineralized Eretmonia macloughlinii from Antarctica. These
fossils demonstrate that at least some Late Permian pollen
organs were simple microsporophyll-bearing shoot systems
and not borne directly on Glossopteris leaves.
Keywords Australia Bowen basin Eretmonia Glossopteris Gondwana Permian
Introduction
Anatomically preserved plant remains from several depositional basins in Australia and Antarctica have provided
significant new information on the glossopterids and other
Gondwanan plants of Late Permian age (Gould and Delevoryas 1977; Pigg and Nishida 2006; Ryberg et al. 2012b;
Schopf 1970, 1976). Studies of the past quarter century in
particular have documented significant anatomical details
for Glossopteris Brongniart leaves and stems (McManus
et al. 2002; Pigg 1990; Pigg and McLoughlin 1997; Pigg
and Taylor 1993; Ryberg et al. 2012a, b), Vertebraria
Royle roots (Gould 1975; Neish et al. 1993), and leaves of
Noeggerathiopsis Feistmantel (McLoughlin and Drinnan
1996). Permineralized ovules and ovulate structures are
known from Antarctica (Klavins et al. 2001; Ryberg 2010;
Ryberg et al. 2012b; Ryberg and Taylor 2013; Smoot and
Taylor 1987; Taylor et al. 1989, 2007) and Australia
(Nishida et al. 2003, 2004, 2007; Pigg and McLoughlin
1997; Pigg and Nishida 2006). Polyembryony has been
documented in some ovules from Antarctica (Ryberg and
Taylor 2013; Taylor and Taylor 1987), while others from
Australia have been shown to have a single embryo and
contain swimming sperm in their micropyles (Nishida et al.
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2003, 2004, 2007). The state of these features is uncertain
in other forms (Ryberg 2010). Several different ovulate and
megasporophyll morphologies are revealed in Antarctica
(Ryberg et al. 2012b) and Australia (Gould and Delevoryas
1977; Nishida et al. 2007), and these have provided the
basis for the interpretation of several different aspects of
glossopterid reproductive biology.
In contrast, the pollen-bearing structures have received
less attention. Although they are found in the anatomically
preserved floras and are illustrated routinely (e.g., Gould
and Delevoryas 1977; Lindström et al. 1997; Schopf 1970),
typically they are poorly preserved and difficult to interpret. Pollen-bearing structures are characterized usually by
a scale-like microsporophyll with a stalk bearing a pair of
branches, typically on the adaxial surface. Each of these
splits into additional branches that ultimately bear clusters
of pollen sacs. This morphological organization is similar
to the morphogenus Eretmonia du Toit. Some anatomical
features of the pollen organ were previously described
briefly by Gould and Delevoryas (1977) and Nishida et al.
(2002) from permineralized specimens from the Bowen
Basin. More detailed structures for pollen bearing structures were interpreted based on permineralized Eretmonia
macloughlinii Ryberg et al. (2012a) from the central
Transantarctic Mountains.
The current study confirms the adaxial attachment of
microsporangiate branching structures to the microsporophyll, and suggests a possible cone-like nature of the entire
pollen organ. The pollen sacs are usually filled with
numerous striate (tanieate) bisaccate pollen grains typically
referred to Protohaploxypinus Samoylovich. Pollen sacs
are fairly shrunken. The microsporophylls are subtended by
several layers of scale-like sterile leaves. Isolated, individual or small clustered groups of pollen sacs that also
occur in the matrix are of the Arberiella type, with black,
thickened and diagonally striate walls, and contain Protohaploxypinus-type pollen.
Anatomically preserved plants from the Homevale Station locality of the Bowen Basin in Queensland, Australia
are among the best preserved of the Late Permian Gondwanan floras. In combination with the previously described ovulate structure, Homevaleia, the present contribution
documents the pollen organ Ediea gen. nov. This distinctive structure shows that at least some glossopterid
microsporangiate structures were cone-like, and not borne
directly on vegetative type Glossopteris leaves.
Materials and methods
Materials used in this study were collected at four exposures at Homevale Station in the Bowen Basin of northeast
Queensland, Australia by Nishida, Rigby and other
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J Plant Res (2014) 127:233–240
collaborators in 1992, 1993 and 1997 (for a locality map,
see Gould 1970). The samples were collected at Nishida
Localities 971 (21° 280 5500 S, 148° 250 0600 E), 972 (21° 280
3500 S, 148° 240 0900 E), and 974 (21° 280 3700 S, 148° 260 0200
E). The meridional locations were identified using OCEA1
geodetic data. The fossils were excavated from the Late
Permian Blackwater Group (Gould and Delevoryas 1977;
McLoughlin 1990a, b, 1992; Pigg and McLoughlin 1997).
Geological and stratigraphical details are available in
Nishida et al. (2004, 2007).
Permineralized rock samples were cut into sections ca.
2 cm thick using a large slab saw. Many blocks were cut
perpendicular to the internal bedding plane, and some of
these were also cut into smaller blocks in order to obtain
serial sections of selected organs. Serial sections were
prepared by the cellulose acetate peel technique using fullstrength, commercial grade (46 %) hydrofluoric acid
(Basinger and Rothwell 1977; Joy et al. 1956). The procedure of preparing microscopic slides was described in
Nishida et al. (2004, 2007). Microscopic slides were
observed by using an Olympus BX 50 transmitted light
microscope and photographed using an Olympus D-20
digital camera. Electronic images were processed using
Adobe Photoshop ver. 7.0.
Peels, slides and original slabs of the holotype specimen
H0001A (Geological Survey of Queensland fossil collection
number GSQF14497) and those of the paratype specimens
illustrated here are deposited at The Queensland Museum,
Brisbane, Australia. Other peels, slides and slabs collected
by us, but not illustrated here, are housed at Faculty of Science and Engineering, Chuo University, Tokyo.
Fig. 1 Ediea homevalensis gen. et sp. nov. Microsporangiate shoot c
and pollen-producing organs. Scale bars for a, b, e, f 1 mm; for
c 5 mm; for d, h, i 0.1 mm; and g 0.2 mm. a Cross section (cs) of
mature shoot showing outer sterile leaves and inner fertile leaves
bearing pollen sacs. Bases of more distal fertile leaves occur around
the main axis at center. Arrowhead indicates an adaxial microsporangiate axis. H0001A #10. b Cs at a more distal level than a,
showing bifurcation of microsporangiate axis (arrowhead), and
better-preserved central axes. H0001A #53. c Longitudinal section
(ls) of mature shoot. Arrow indicates base of shoot axis. H93010Bbot
#10. d Scalariform tracheids in the shoot axis in (c). e Oblique section
of shoot filled with immature microsporangiate organs. Arrowheads
indicate two expanded microsporangiate axes; distal portion of each
axis is shown by arrowheads with white inside. 5Y-OQWside #6. f Cs
of youngest microsporangiate shoot. Serial numbers indicate spiral
phyllotaxy. Some microsporophylls have an adaxial pair of immature
pollen-bearing structures (p), and leaf 9 (arrowhead) has a possible
residue of the same structure. H393031E2top #2. g Central part of
e enlarged, showing main axis (ax), a departing fertile-leaf trace (Lt)
and one of fertile leaves (L1). Contours of main axis and illustrated
leaves are in red and yellow, respectively. Arrowheads as in (e).
h Enlargement of Lt in slightly distal 5Y-OQWside #7, consisting of
three traces (yellow arrowheads), and leaf gap margins (red
arrowheads) of main axis (ax). i L1 in g enlarged, showing three
vascular bundles in leaf base (yellow arrowheads)
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Results
Systematics
Class Glossopteridopsida Banerjee 1984
Order Glossopteridales Banerjee 1984
Family Glossopteridaceae
Genus Ediea H. Nishida, Pigg, Kudo et Rigby gen. nov.
(Figs. 1, 2, 3)
Previous illustrations Gould and Delevoryas 1977
Generic diagnosis Anatomically preserved gymnosperm
microsporangiate shoot composed of main axis, proximally
produced sterile leaves and distally borne microsporophylls; main axis eustelic, leaves diverging in helical
phyllotaxy; sterile leaves elliptical, thin, scaly, sessile,
lamina narrower apically, broader distally, margins overlapping, slightly incurved adaxially; microsporophylls
narrower than sterile leaves, bearing paired fertile axes on
adaxial surface; fertile axes vascularized, continuously
bifurcating distally terminating in microsporangia in helices or whorls; pollen bisaccate, sacci reticulate, corpus
striate.
Type species Ediea homevalensis H. Nishida, Pigg,
Kudo et Rigby sp. nov.
Species diagnosis Shoot elongate-elliptical, *30 mm
long, 4 mm in diameter in mature stage; sterile leaves
5 ? 10, microsporophylls 5 ? 8 in number; leaves
diverging in 3/8 phyllotaxy; microsporangiate axis
[1.2 mm long; mesophyll cells mostly rounded, parenchymatous and of generally uniform size; tracheids scalariform; pollen bisaccate, striate, and 30–36 lm wide;
corpus, 15–17 lm in diameter.
Holotype The Geological Survey of Queensland fossil
collection number: GSQF14497 (Original collection number H0001A)
Paratypes GSQF14498 (Original collection number:
H393031E2), GSQF14499 (5Y-OQW), GSQF14500
(H93010B)
Stratigraphic position Blackwater Group, Bowen Basin,
Queensland, Australia; Upper Permian.
Etymology The generic name Ediea, is in honor of Dr.
Edith L. Taylor for her many contributions to our understanding of Glossopteris and associated Gondwana floras.
The species name, homevalensis, refers to the collecting
locality at Homevale Station, Queensland, Australia.
Description
Pollen-bearing structures of Ediea homevalensis are of
several sizes (and presumably developmental stages) and
levels of preservational detail. Some specimens are mature
strobili similar to those described and illustrated previously
by Gould and Delevoryas (1977), but with better preserved
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Fig. 2 Ediea homevalensis gen. et sp. nov. Microsporangiate shoot c
and pollen-producing organs. Scale bars for a, b 1 mm; for c 0.1 mm;
and e, f 10 lm. a–d Serial sections of more distal part of 5Y-OQW
shown in Fig. 1a. a, c 5Y-OQWside #25. b, d 5Y-OQWside #51. a Cs
of lower half of shoot, showing proximal part of L2 bearing an adaxial
microsporangiate axis (arrowhead). Some histological details of
sterile leaves are preserved in part. b Distal part of L2 and the same
microsporangiate axis (arrowhead). c Enlargement of L2 in a,
showing three vascular bundles (yellow arrowheads) and connection
of microsporangiate axis (black arrowhead) to a bundle at left.
Arrowhead with black margin indicates distal portion of the same
axis. d Distal portion of L2 with laterally expanding incurved margins
and three bundles (yellow arrowheads). Note that a whorled cluster of
microsporangia adaxial to L2 comes from axis different from the one
attached to L2 (black arrowhead). e, f Various views of in situ pollen
grains, showing features of Protohaploxypinus-type dispersed grains.
H0001A #55
microsporophylls bearing pollen sacs filled with pollen
grains (Fig. 1a–c). Another specimen is of a younger
strobilus (Fig. 1e), and a third one is a young shoot sectioned transversely near the apex. These last two specimens
document a 3/8 phyllotaxy (Fig. 1f). Together, these
specimens provide the basis for understanding the structure
of these microsporangiate organs.
The smallest specimen is a shoot about 2 mm in diameter that is sectioned transversely near the apex (Fig. 1f).
Fourteen leaves are helically arranged around a central axis
in a 3/8 phyllotaxy. Of these, the inner nine are interpreted
as microsporophylls bearing immature pollen sacs and the
outer five are sterile and scale-like (Fig. 1f). The sterile
scale-like leaves are thin and wide, around 0.05 mm thick
and characterized by mostly uniform mesophyll cells. In
contrast, the microsporophylls are narrow and thick,
attaining around 1 mm thickness, thickest at a central
midrib area with thinning margins that curve slightly
inward. The microsporophyll tissues are mostly composed
of parenchymatous cells, but usually poorly preserved.
Pollen sacs are attached to the adaxial surfaces of microsporophylls by small elongate stalks that terminate a
cluster of black bodies that are comparable with immature
microsporangia based on morphological similarity to other
mature organs and on inferred developmental sequences
(Fig. 1f). The leaf numbered 9 in Fig. 1f is interpreted here
to be a much more developed fertile leaf in the shoot,
judging from the presence of a spongy tissue on its adaxial
side and comparatively thinner and wider appearance of
fertile leaves in later developmental stages (Fig. 1a–c).
While the youngest shoot shows only a pair of unbranched
clusters of microsporangiate organs, others have more
extensively branched aggregates of sporangia.
A second, larger specimen is a shoot ca. 3.5–4 mm in
diameter. The axis bears around five to six helically
arranged sterile, outer scale-like leaves surrounding a
rather loosely arranged helix of fertile leaves with clusters
of possible pollen sacs (Fig. 1a, b). The number of fertile
J Plant Res (2014) 127:233–240
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leaves is uncertain. The scale leaves are wider than the
fertile leaves, but the entire thickness of the two structures
does not differ much. Leaves are thickest at the midrib
where one larger bundle is located at the basal portion of
leaf. In fertile leaves the base of the adaxial microsporangiate stalk is also thickened (Fig. 1a, b). Mature leaves
have an epidermis and mesophyll composed of uniform
parenchyma. Abaxial tissues of one fertile leaf immediately below the microsporangiate stalk are degenerated,
leaving a large space in the mesophyll (Fig. 1a, b). Judging
from comparison with other specimens, the space is not
interpreted to be a histologically differentiated structure,
such as a secretory cell or resin canal. Details of laminar
vasculature in distal portion of leaves were not confirmed.
Fig. 3 Suggested reconstruction of Ediea homevalensis gen. et sp.
nov.
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There are 40–50 pollen sacs within a given transverse
section. Another specimen at a similar developmental stage
is sectioned longitudinally, and is 30 mm long and 4 mm
wide (Fig. 1c). The main axis at the base of the fertile shoot
contains tracheids with scalariform thickenings (Fig. 1e).
The fertile leaves are appressed to the main shoot, have a
wide basal lamina, and lack a prominent petiole. A pair of
slender stalks, each vascularized with scalariform tracheids, project from the adaxial surface of a fertile leaf
(Fig. 1a, b). The stalk first bifurcates at about 1 mm from
its base (Fig. 1b). After branching several times further,
each branch terminates in a pollen sac, resulting in two
relatively dense clusters of microsporangia. Each pollen
sac is filled with bisaccate, striate pollen grains. The sporangial wall consists of small cells containing a black
substance, and is diagonally striated in surface view similar
to the Arberiella-type microsporangia (Fig. 1b).
A third type of specimen of the more typical preservation is an unexpanded shoot 6.8 mm long and 1.5 mm wide
that is slightly crushed on one lateral side toward its apex
and has been sectioned obliquely with 51 serial peels.
Although the tissue preservation is incomplete, this specimen is interpreted as a central axis bearing ca. 10 outer
sterile leaves and at least five inner fertile leaves, including
a diverging leaf base (Fig. 1e, g–i). Numerous pollen sacs
fill the space between the central axis and the fertile leaves
(Fig. 2a, b). The pollen sacs can be recognized by the dark
contour of their external walls (Fig. 2a–d). They are
smaller than mature ones and are crushed, lacking cellular
contents. In the microsporangiate cone at this developmental stage the epidermis of the main axis and of the
leaves is also filled with dark substances, making it easier
to follow external contour of each organ even when the
ground tissues are mostly degenerated (Fig. 1g).
Cells of leaf tissues are generally poorly preserved, but
better histology can be observed for sterile leaves than the
fertile ones. The sterile leaves have a mesophyll that is
composed of thin-walled parenchyma on the adaxial side,
and one to several layers of thick-walled cells of an abaxial
hypodermis that give each leaf a darker abaxial outline.
The sterile leaves are thickest in the middle, where a larger
vascular bundle exists (Fig. 2a, left side), and gradually
taper on both lateral margins. The fertile leaves are narrower, but have a thicker mound-like central portion particularly close to the leaf base, where cells are mostly
degraded except for residues of three vascular bundles
(Fig. 2c, d). The fertile leaf abruptly tapers from the central
mound to both lateral margins, curving adaxially and
steeply inward.
The main axis is poorly preserved, but the stele is represented as a pair of thin plates of xylem, partly dissected
because of a possible additional leaf gap (Fig. 1g). Three
leaf traces are produced in a single gap between the cauline
J Plant Res (2014) 127:233–240
sympodia (Fig. 1g, h). Leaf traces of the microsporophylls
first have a single bundle, which divides laterally on either
side resulting in three bundles at the leaf base (Fig. 1h).
More proximal fertile leaves are found in sections in the
series of microscopic slides. They are mostly crushed and
disorganized, but some showed structural details (Figs. 1g,
i, 2c, d). The fertile leaves also have three bundles at their
base. Further division of the leaf vascular bundles was not
confirmed because of poor preservation.
Microsporangiate axes are branched repeatedly, with a
slender, elongate stalk composed of parenchyma and vascular tissues with scalariform tracheids as observed in the
mature axis. Each axis terminates in a microsporangium.
Microsporangia are aggregated distally on highly branched
axes in a tight helix or in a whorl of more than five sporangia (Fig. 2b, d). One microsporangiate stalk is found in
attachment to the adaxial side of the outermost vascular
bundle of the three (Fig. 1c).
Pollen is of the Protohaploxypinus-type, 30–36 lm wide
with a central body (corpus) 15–17 lm across with
prominent horizontal striae (Fig. 2e, f). The paired sacci
are around 7 lm across and characterized by conspicuous
reticulate pattern on the inside of the tectum (Fig. 2e). The
areole diameter of the endoreticulations varies from 2.0 to
3.7 lm.
Discussion
The new fossil-taxon Ediea homevalensis gen. et sp. nov.
adds new evidence concerning anatomical details of a
glossopterid microsporangiate cone bearing Eretmoniatype microsporophylls. We here propose the new genus
Ediea, on the basis of specimens that clarify the monosporangiate shoot nature of one glossopterid pollen-bearing
structure. This material documents details of developmental sequences of the shoot that became over 3 mm long
when mature.
The distinctive features of Ediea include the eustelic
stem, leaves in 3/8 phyllotaxy, the proximal (external)
sterile leaves ca. 5–10 in number, the distal fertile leaves
ca. 5–9 in number, the three traces in the base of microsporophylls, the adaxial pair of vascularized microsporangiate branches terminating in Arberiella-type sporangia, the
mostly parenchymatous mesophyll, and the Protohaploxypinus-type pollen grains. The three leaf-traces to
the microsporophyll probably derive from a single trace,
which divides to produce a trace on either side. This
venation pattern is similar to that observed for Homevaleia,
the megasporangiate organ from the same fossil assemblage (Nishida et al. 2007).
Ryberg et al. (2012a) described a pollen-bearing conelike structure from the Late Permian of Antarctica similar
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to Ediea homevalensis, as Eretmonia macloughlini. The
name Eretmonia is usually used for impression–compression fossils in which the distinctive features described here
could not be observed. Conversely, our material of Ediea
lacks evidence of the external morphology and the anastomosing venation patterns typical for Eretmonia. We,
therefore, prefer to establish a new genus for the permineralized fossils based on anatomical structures, and in
accordance with the International Code of Nomenclature
for algae, fungi and plants, Art. 1–2 (Melbourne Code
2012).
Ediea homevalensis shares many features with Eretmonia macloughlinii, both are simple pollen cones with similar shoot organization, position and number of
microsporangiate axes on the microsporophyll, scalariform
tracheids, pollen-sac and pollen morphologies. On the
other hand, Ediea homevalensis differs from Eretmonia
macloughlinii in several respects––the microsporophylls
lack large secretory canals in the mesophyll that have been
reported for Eretmonia macloughlinii. Furthermore, the
three vascular bundles enter a broad leaf base that lacks a
distinct petiole. In situ pollen grains are morphologically
similar to each other in the two species, but are nearly half
the size in Ediea homevalensis (30–36 lm wide vs. around
80 lm). These differences are enough to recognize the two
species of pollen cones as representatives of separate species and suggest that they were borne by different glossopterid plants. In contrast to the wide morphological
diversity found in glossopterid megasporangiate organs
from the Late Permian of Antarctica and Australia (Ryberg
et al. 2012b), the microsporangiate organs seem to be less
diversified based on the evidence at hand to date.
The ovule-bearing megasporophyll Homevaleia is often
associated with Ediea even on the same microscopic slide.
Although the histological composition of Ediea leaves is
not fully understood, they are similar to the Homevaleia
megasporophylls in the presence of a hypodermis composed of thick-walled cells to the abaxial side, and parenchymatous mesophyll to the adaxial side (Nishida et al.
2007). It is highly probable that Ediea pollen cones were
produced by the Homevaleia plant.
Combining anatomical features observed from specimens representing three successive developmental stages,
we suggest a tentative reconstruction of Ediea (Fig. 3). The
external morphology is similar to an impression-based
genus, Squamella Surange et Chandra. A 3D reconstruction
supported by computer software could provide additional
realistic images of specimens in the future. The evolution
of microsporangiate organs of the seed plants are less
clarified in comparison to that of megasporangiate organs.
Ediea provides firm evidence on the morphology of a
glossopterid microsporangiate organ and its fertile component that traditionally called a microsporophyll. The new
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evidence provides a basis for modifying and improving
systematics and for reconstructing phylogenies of the
glossopterids and the seed plants. Further discussions on
the morphological and evolutionary interpretation of the
glossopterid reproductive organs in combination with megasporangiate organs will be presented elsewhere.
Acknowledgments The field collection at Homevale was supported
by Grants for Overseas Survey 04041034 from MEXT, Japan to Prof.
Emeritus Masahiro Kato, The University of Tokyo, and 08041135 to
Prof. Motomi Ito, The University of Tokyo to whom we are deeply
grateful. This study was supported in part by Grant in Aid for Scientific Research 07640933 from MEXT to H.N., and by National
Science Foundation Grant BSR-9006625, and an Arizona State University Faculty Grant-in-Aid to K.B.P. Special thanks are also due to
two distinguished reviewers, Prof. Gar W. Rothwell and Prof. James
A. Doyle for their appropriate comments and suggestions.
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