THE UMVERSITY
OF ILLINOIS
LIBRARY
ILL
ILLINOIS BIOLOGICAL
MONOGRAPHS
Volume XIII
PUBLISHED BY THE UNIVERSITY OF ILLINOIS
URBANA, ILLINOIS
EDITORIAL COMMITTEE
John Theodore Buchholz
Fred Wilbur Tanner
Charles Zeleny, Chairman
TABLE OF CONTENTS
NUMBERS PAGES
1. Studies on Some Protozoan Parasites of Fishes of Illinois.
By Richard Roksabro Kudo 1
2. The Papillose Allocreadiidae — A Study of Their Morphology.
Life Histories, and Relationships. By Sewell Hepburn
Hopkins 45
3. Evolution of Foliar Types, Dwarf Shoots, and Cone Scales of
Pinus, with Remarks Concerning Similar Structures in Re-
lated Forms. By Clifton Childress Doak 125
4. A Monographic Rearrangement of Lophodermium. By Leo Roy
Tehon 231
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ILLINOIS BIOLOGICAL
MONOGRAPHS
Vol. XIII No. 3
EDITORIAL COMMITTEE
John Theodore Buchholz Fred Wilbur Tanner
Charles Zeleny
Published by the University of Illinois
Under the Auspices of the Graduate School
Urbana, Illinois
Distributed
August 6, 1935
UNIVERSITY
ILLINOIS
1000—8-35—5791 .. press
EVOLUTION OF FOLIAR TYPES, DWARF
SHOOTS, AND CONE SCALES OF PINUS
With Remarks Concerning- Similar Structures in
Related Forms
WITH THIRTY-TWO TEXT-FIGURES
BY
Clifton Childress Doak
Contribution from the Botanical Laboratory of the
University of Illinois
ACKNOWLEDGMENT
The writer gratefully acknowledges the
guidance, helpful suggestions, and criti-
cisms which were furnished by Dr. John
T. Buchholz, Professor of Botany at the
University of Illinois, during the prog-
ress of these investigations.
CONTENTS
PAGE
I. Introduction 7
A. Review of Literature . 7
B. The Problem 8
C. Materials and Methods 10
D. Definition of Terms 10
II. The Vegetative Long Shoot 12
A. Simple Leaves of the Long Shoot 12
1. Cotyledons 12
2. Juvenile and Traumic Simple Leaves .... 14
B. Bud Scales, Sterile Bracts, and Subtending Scales. . 19
C. Homologies of the Axillary Shoots 31
D. Normal Annual Growth of the Vegetative Long Shoot 31
E. Abnormal Annual Growth of the Long Shoot ... 33
1. Multinodal Annual Growth and Summer Shoots . 33
2. Lateral Cones 35
3. Intrusion of Ovulate Cones into Staminate Cone
Series 35
4. Abnormal Axillary Bud Development .... 37
III. The Reproductive Long Shoot, or Ovulate Cone Axis . . 37
A. Primary Foliar Organs 37
B. Growing Point 39
IV. The Evolution of the Long Shoot 42
A. The Vegetative Long Shoot and Its Foliar Organs . 42
B. The Ovulate Long Shoot, or Cone Axis 42
V. The Vegetative Dwarf Shoot and Its Foliar Organs . . 43
A. Sheath Scales 45
1. Morphology 45
2. Methods of Scale Removal 49
3. Scale Number per Dwarf Shoot 50
4. Axillary Structures 55
B. Functional Leaves, or Needles 55
1. Time of Deposit 55
2. Leaf Orientation 57
3. Leaf Fusions 57
4. The One-Leafed Pine (Monophylla) .... 61
5. Leaf Reduction in Monophylla 62
6. Leaf Reduction in Other Pines 63
B. Functional Leaves, or Needles (continued) page
7. Increases in Leaf Number 64
8. Factors Determining Leaf Number 66
9. Vascular Supply to the Leaves 68
C. Meristematic Tip, or Bud of the Dwarf Shoot. . . 68
1. Abnormal (Proliferated) Interfoliar Buds ... 68
2. Normal (Non-Proliferated) Interfoliar Buds . . 69
D. Branch and Leaf Forms in Fossil and Modern Relatives
of Pin us 72
1. Pityites 72
2. Prepinus statenensis 73
3. Fossil Pines of Modern Types 74
4. Taxites 74
5. Pityophyllum 75
6. Modern Relatives 75
VI. Evolution of the Vegetative Dwarf Shoot and Its Foliar
Organs 76
A. Literature 76
B. Steps in the Evolution of the Dwarf Shoot and Func-
tional Leaves 77
C. Evolution of the Leaf Meristems 81
VII. The Ovulate Dwarf Shoot, or Seed Scale 82
A. Voltzia and the Primitive Type of Seed Scale ... 82
B. Developmental Morphology of the Normal Seed Scale 83
C. Abnormalities of Bisporangiate Cones 84
D. Abnormalities of Monosporangiate and Proliferated
Cones 88
E. Vascular Supply and the Scale of Araucaria ... 91
VIII. Evolution of the Ovulate Dwarf Shoot, or Seed Scale . . 92
A. Leading Interpretational Theories 92
B. Summary of Steps in Cone Scale Evolution ... 95
C. Advantages of the Brachyblast Interpretation. . . 96
IX. The Phylogeny of the Pinaceae 97
X. Summary 99
Bibliography 103
I. INTRODUCTION
A. Review of Literature
Since the dawn of botany as a science, the Gymnosperms have been
of special interest; and the genus Pinus, because of its wide distribution,
its economic importance, and its highly specialized dwarf shoots, has
probably attracted more investigators than any other genus among
gymnosperms. Hundreds of special papers dealing with this subject have
appeared, the most important of which will be cited in connection with
the special topics of which they treat. Numerous general works either in-
clude Pinus or deal with this genus alone. A modern and nearly complete
list of the general works will be found in A Handbook of Conifcrac, by
Dallimore and Jackson (24).* Since the present paper deals with both
the foliar and axial systems of pines, much of this extensive literature
has either a direct or an indirect bearing on the present problem.
Some of the most important early works in the field of pines were
done by Lambert (50) and Engelmann (30) from whose works early
literature lists may be obtained.
The embryo and cotyledons have been the subject of special studies or
have been included in the works of Goethe (40), Richards (72), Engel-
mann (30), Daguellion [2i), Tubeuf (93), Masters (57), Buchholz (13,
14), and others.
The seedling stages were treated by Menge (62), Beissner (5),
Masters (57), Hill and DeFraine (41), and numerous others, while the
buds and bud scales have been made the objects of special investigations
by a long list of workers including Schumann (80), Lord Avebury (54),
and Masters (57).
The interpretation of the cone scales has been the subject of a con-
troversial and almost endless literature. Some of the chief contributors
in this field are Robert Brown (12), Alexander Braun (11), Baillon (2),
Sachs (75), Willkomm (101 and 102), Celakovsky (20), Schleiden (78),
Parlatore (68), Velenovsky (97), Von Mohl (99), Strasburger (87),
Aase (1), Saxton (76), and a host of others.
The literature dealing with the dwarf shoot is not so extensive. Im-
portant morphological contributions have been made, however, by Mast-
ers (57), Thompson (91), Schneider (79), and a few others, while im-
portant contributions from the fossil records have been made by Jeffrey
(46) and Seward (81).
* Numbers following names of authors refer to items in the Bibliography at the end of
this paper.
s
ILLINOIS BIOLOGICAL MONOGRAPHS
[132
B. The Problem
During the accumulation of the mass of literature now available much
has been learned of the genus Pinus and its affinities. Much of this in-
formation, however, exists as detached fragments. The great need is for
consolidation, supplementary investigation, and re-interpretation. With
these needs in view the present work was undertaken. As the investiga-
tion progressed it became obvious that a detailed study of the ontogeny
and morphology of the entire axial and foliar systems would contribute
materially to a better interpretation of the phylogeny and affinities of the
genus. The problem as thus broadened involves consideration of a highly
1 1.
E.
K
G.
II'
I.
J.
K.
Fig. 1. — Stem units of
Cotyledonary units.
Simple-leafed juvenile unit.
Fertile units.
C. Branch bud unit.
C 2 . Dwarf shoot unit.
C 3 . Staminate cone unit.
C. Ovulate cone unit.
C 5 . Seed scale unit.
Bud scale unit.
Sterile bract unit.
Sheath scale unit.
Functional leaf or needle unit,
and H 2 . Involucral scale units.
Microsporophyll unit.
Megasporophyll unit.
Semi-diagrammatic view o[ a stem
tip during deposit of fertile units.
The subtending scales have been
removed in order to show the
young dwarf shoots.
pine (and miscellany).
L. Diagram of denuded dwarf shoot
of P. Strobus showing base of
growing leaves. The sheath
scales have been removed.
M. Same showing mature leaves and
well-formed "pulvinus."
N. Diagram of axial plane passing
through both the long shoot and
the dwarf shoot. Lateral and sub-
tending scales are also shown.
O. A two-needled dwarf shoot with
one of the needles aborted.
R. Diagram showing components of a
fertile stem unit.
133] EVOLUTION OF PINUS—DOAK 9
specialized, polymorphic branch system and an even more highly complex
system of specialized structures which are the morphological equivalents
of leaves.
Since the acceptance of the idea that the fascicle is borne on a dwarf
shoot, it has been known that pines exhibit an extreme case of dimor-
phism of the vegetative branches. The possession of specialized, decidu-
ous, dwarf shoots in contradistinction to the long shoots, is now univer-
sally accepted as the chief distinguishing character of the pines.
The modified branches which serve as axes for the staminate and
ovulate cones respectively are not of the same order and are not, there-
fore, homologous.
According to the widely accepted "Brachyblast Theory," the seed scale
also represents a modified branch; hence the branches of Pinus are not
dimorphic but polymorphic, there being a total of five types as follows:
(1) long shoot; (2) dwarf shoot; (3) staminate cone axis; (4) ovulate
cone axis; and (5) seed scale axis.
In addition to this complex branch system, there are developed in the
course of the ontogeny of each pine tree at least eleven types of special-
ized leaf structures. These were in part described by Engelmann (30),
who recognized seven types exclusive of the sporophylls. Dufrenoy (27)
pointed out the fact that in some ancestors of pine, the undifferentiated
leaves likely served the triple functions of spore formation, carbon as-
similation, and protection of the meristematic tips. By way of specializa-
tion to serve one of these functions or some combination of them, the
organs here listed, in order of their ontogenetic appearance, have evolved.
1. Cotyledons (Fig. 1 A).
2. Simple, primary or juvenile leaves (Fig. IB).
3. Bud scales (Fig. ID).
4. Sterile bracts of the main axis (Fig. IE).
5. Fertile or subtending bracts of the main axis.
a. Subtending branch buds (Fig. 1 CM.
b. Subtending short shoot (Fig. 1 C 2 ).
c. Subtending staminate cones (Fig. 1 C 3 ).
d. Subtending ovulate cones (Fig. 1 C 4 ).
6. Fascicle sheath scales (Fig. IF).
7. True or needle leaves (Fig. 1 G).
8. Involucral bracts for the cones.
a. For staminate cones (Fig. 1H 1 ).
b. For ovulate cones (Fig. 1 H 2 ).
9. Microsporophylls (Fig. II).
10. Cover scales or bracts for the seed scales (Fig. 1 C 5 ).
11. Megasporophylls (Fig. 1 J).
10 ILLINOIS BIOLOGICAL MONOGRAPHS [134
The scope of the problem as outlined here is so broad that the present
paper must necessarily include numerous separate short investigations
undertaken either to supplement and round out data already available or
to bridge the gaps between bodies of existing knowledge. In the light
of these investigations, the author hopes to summarize and re-interpret
some of the controversial questions raised by the work of other investiga-
tors. Obviously, too, any consideration of phylogenetic relationships must
involve other genera, both paleontological and extant.
C. Materials and Methods
The materials for this study were taken from pines of about thirty-
five species gathered from widely separated points throughout the United
States and neighboring islands. Many European and Asiatic forms which
are now growing under cultivation in America are included. The most
detailed studies were made on P. sylvestris L., P. Laricio var. austriaca
End., P. cembroides var. monophylla Voss., P. tacda L., P. Pinaster Ait.,
P. palustris Mill., and P. Strobus L. In all of these species the observa-
tions extended over either two or three growing seasons.
Seeds, buds, and other parts were dissected under a binocular dissect-
ing microscope ; and those parts which the binocular revealed as being of
possible histologic interest were later imbedded and sectioned.
For the major subdivisions of the Conifcreae, the writer has followed
the classification used by Coulter and Chamberlain (22). The specific
names of the various pines have been taken from Dallimore and Jack-
son (24).
D. Definitions of Terms
A stem unit is considered in this paper to be an internode, together
with the node and nodal appendages at its distal extremity (Fig. 1 R).
It consists of an allotted portion of a stem (internodal component), a
poorly defined node, a modified or unmodified leaf (foliar component)
which may or may not subtend an axillary outgrowth (axillary com-
ponent). A unit without an axillary component is said to be sterile.
The term node is used in its usual sense; but since the term multi-
nodal has been used (see Shaw, 82) to describe the annual growths which
show more than one period of deposit in a single season, the term is re-
tained in this sense even at the risk of some confusion. It is to be
remembered, however, that the term multinodal refers not to a plurality
of nodes but to a plurality of periods of deposit.
In the literature the terminal bud of the dwarf shoot, because of its
position with reference to the needles, has been termed the interfoliar bud
in which sense the term is here retained.
135]
EVOLUTION OF PINUS—DOAK
11
The term dwarf shoot is applied to the modified branches which in the
literature are often called by various other names such as spur shoot,
short shoot, and brachyblast. The term fascicle is reserved for the tuft
of needles on a dwarf shoot and is thought of as being separate from the
sheath of scales (f ascitic slicath) around the needles.
By deposit is meant the instant of earliest recognition of a primor-
dium.
The term bud scale is used in its restricted sense and is applied to
those closely spaced, sterile-axiled, scale-like, primary foliar organs which
serve only as protective cover for the buds.
By extension is meant the enlargement of a structure to its final size
(second growth phase). The year's growth is that portion of a long shoot
of which the units are extended during a single growing season.
The term perforation is applied to the growth of other parts through
a scale (Fig. 11 C, C, and D'). The term axial plane is applied to a
plane passing through the long axes of both a dwarf shoot and the long
shoot to which the short shoot under consideration is attached (Fig. 1 N,
a-p).
A primordium formerly present but no longer appearing is considered
to have been suppressed ; if the rudiment appears and is then lost without
differentiation of vascular tissues, the structure is said to be incorporated.
If the structure represented by a primordium loses its identity as a sepa-
rate organ but, as a constituent of a connate structure, differentiates a
separate vascular supply, it is considered to have been welded into a now
compound structure.
The seed scale can be shown to consist of more than one foliar unit;
for this reason the term sporophyll is applied to the morphological spore-
bearing leaf which forms only a part of the seed scale. The term seed
scale, therefore, is reserved for the entire seed-bearing structure.
STERILE SERIES
FERTILE SERIES
Fig
2. — Diagram of a compound winter bud of pine, showing condition
of units, order of deposit, and order of extension.
12 ILLINOIS BIOLOGICAL MONOGRAPHS [136
II. THE VEGETATIVE LONG SHOOT
A. Simple Leaves of the Long Shoot
The order of appearance of the various units which make up a pine
tree has been given above. We shall now consider each type of unit in
the light of the observations made during the present study. The first
leaves to appear are always of the simple type. These are usually glau-
cous and, with the exception of the cotyledons, have toothed margins
(Fig. 5 C and Fig. 6 C) even in species whose functional leaves are
entire. They are broadened laterally, especially at their bases. They are
keeled and never grow for long periods from zonal meristems, as do the
regular needles, but mature all their tissues at approximately the same
time. Simple leaves are not confined to the vegetative long shoots but
occur also on dwarf shoots and even on the cone axes. In the course of
the present work, during which hundreds of branches were examined, a
close watch was kept for possible simple leaves. Numerous cases were
found which, when analyzed, fell under one of the types listed below.
1. Cotyledons
The first simple leaves to appear are the cotyledons about which there
has accumulated an extensive literature. It is generally agreed that the
cotyledons are conservative in characters and, since they themselves are
simple, are indicative of a simple-leaved ancestor for the genus Piiuts.
As early as 1817 Goethe (40) argued that if a leaf is not to be
thought of without a node or a node without a bud, the cotyledons, since
they are leaves, mark the first node of a plant. He accounted for their
cyclic arrangement and sterile axils by assuming a phylogenetic loss of
both internodes and axillary buds. The essential correctness of these in-
terpretations is borne out by the occasional assumption of a weak spiralled
arrangement as reported by Buchholz (13, 14), or by the occurrence of
buds in the axils of the cotyledons as found by Richards (72).
In following the early ontogeny of the cotyledons, Buchholz (13) has
shown that the meristem of the stem tip arises in the embryo before the
cotyledonary primordia are laid down. This differentiation of meristem
for the plumule marks the beginning of the long shoot, and the appear-
ance of the cotyledonary primordia upon it marks the beginning of its
first foliar appendages. In the papers just cited, Buchholz shows that
two or more cotyledonary primordia often "fuse" and give rise to a single
cotyledon (Fig. 7 C, D, E, and F). He describes broad cotyledonary
primordia of possible double nature and also undoubted double primordia
which, without leaving a trace of their former bivalence, develop into
simple structures. My own investigations have revealed similar processes
137] EVOLUTION OF PINUS—DOAK 13
in P. tacda. They are probably of common occurrence among other poly-
cotyledonous forms. Buchholz and Old (16), in their work on embryos
of a close relative of Pinus, express the view that the cotyledonary tubes
observed by Hill and DeFraine (41, 42) in the seedling stages of Ccdrns
atlantka were produced by intercalary growth during germination. The
degree of adhesion attained in the formation of such tubes indicates that
fusions can occur either early or late in cotyledonary ontogeny and that
the union can be either complete (primordia incorporated) or partial
(structures welded).
In order to bring about incorporation the primordia are deposited as
is normal for growing points. Meristematic activity, however, instead of
being confined to these — which would result in the production of separate
organs — spreads laterally and recedes toward the base until all the inter-
vening and subjacent tissues are involved. Two or more adjacent pri-
mordia are thus lifted up by a common (intercalary) growth. At first
the resulting compound structure has as many growing points as there
were constituent primordia. Some of the points, however, are soon in-
corporated and their separate identity is lost. Hence the mature organ
is usually univalent, and there is no trace of the double or triple nature of
its early ontogeny. From such evidence obtained in work on the embryos
of P. Banksiana, Buchholz concludes that there is in this species a distinct
tendency to reduce the cotyledons.
That this phenomenon is not confined to P. Banksiana, and that the
incorporation of one organ by another is not always complete, is shown
by the frequent occurrence of double, bivalent, or welded cotyledons as
described by Hill and DeFraine (41, 42).* These workers show that the
union may involve a part or all of the cotyledons, the latter condition pro-
ducing a hollow cylindrical cotyledonary tube. Such tubes were reported
as occurring regularly in five species of pines and in several other gymno-
sperms.
Since the results just described are nothing more than different ex-
pressions of the same fusion phenomenon, it is significant, but not sur-
prising, that double cotyledons and occasional cotyledonary tubes are
found in the same species. What is more significant is that, for those
pines (P. contorta var. Murrayana, and P. montana var. gallica) showing
both fused cotyledons and occasional cotyledonary tubes, the total number
of maturing cotyledons is far lower than occurs in pines generally. Of
*Curiously enough these workers interpreted the partly divided cotyledons as evidence
that, by division, the dicotyledonous condition, which they held to be primitive, was giving
rise to polycotyledony. As pointed out by Coulter and Chamberlain, however, the partly fused
condition can be used with equal force to show that by fusion of members the primitive poly-
cotyledonous condition is giving rise to the condition of dicotyledony. The fact that primordia
were observed to fuse, not only in Pinus, but in several other polycotyledonous genera, makes
it probable that polycotyledony is primitive and dicotyledony derived, which is the view of the
present writer.
14 ILLINOIS BIOLOGICAL MONOGRAPHS [138
all species studied by Hill and DeFraine, the prevailing cotyledonary
numbers ran -12-11-10-9-9-8-7-6-4-4-4-, and yet the number occurring in
the two pines which showed both these conditions was in each case four,
the lowest number in the series. These facts are strongly suggestive of
fusion and incorporation as the means by which the reduction to this low
number has been accomplished. This is in keeping with the theory of a
generalized tendency toward reduction which Coulter and Chamberlain
(22) have set forth for all gymnosperms.
It is apparent that the ontogeny of adjacent cotyledonary or other
primordia can follow any one of three courses. The usual course is for
each primordium to grow into a separate structure ; this, of course, in-
volves no reduction. Either of the other methods, however, results in
fewer mature organs than beginning primordia. If, by intercalary growth,
two or more primordia are lifted on a common structure, as described
above, and each constituent later differentiates its own vascular supply,
the effect is to produce a reduced number of organs which are clearly
bivalent, or connate, as are the cotyledons of a cotyledonary tube. How-
ever, since the vascular supply to pine cotyledons is usually simple, this
cannot be the means by which cotyledonary reduction is being accom-
plished in Pinus.
The third possibility involves reduction by elimination of primordia
through complete incorporation as described above.
The tendency toward the elimination of foliar primordia by meristc-
matic recession and incorporation is not confined to the cotyledons but
manifests itself at many points in the ontogeny of a pine tree, and, as will
be shown later, it is by this process that the stem tip and extra leaf pri-
mordia are eliminated from the dwarf shoots of P. cembroides var. mon-
ophylla. The fusion of parts of the Abietineous cone scale and the elimi-
nation of parts from this structure are also explainable on similar
grounds. For these reasons it is not alone the evidence of reduction but
also the manner of reduction which assumes importance in the present
paper.
2. Juvenile and Traumic Simple Leaves
Above the cotyledons the seedlings of all pines are at first clothed
with simple leaves, as shown by Menge (62), Coulter and Chamberlain
(22), and many others. The simple leaves are spirally arranged along
the long axis, a character which is held in common with all Abietineae.
The simple leaves are followed eventually by scales and other special-
ized foliar organs (Fig. 1). The early botanist rightly attached signifi-
cance to this sequence and used it as an argument for the derivation of
specialized leaves from the simple type. Beyond the seedling stages,
139]
EVOLUTION OF PINUS—DOAK
IS
Fig. 3. — Proliferated dwarf
A. Interfoliar buds of P. Laricio.
B. Proliferated fascicle of P. Laricio
with simple subtending leaves,
withered original needles (s) and
three-needled fascicles (y).
C. Xylem cylinder from a young twig
showing naked portion in posi-
tion of former bud scale scar.
shoots (and miscellany).
D. Interfoliar buds of P. Strobus.
E. An annual growth node of P. Lari-
cio showing scars of the differ-
ent units ; m and n represent bud
scale scars.
F. Simple green leaf from B.
G. Shed lateral scale from B.
lb ILLINOIS BIOLOGICAL MONOGRAPHS [140
simple leaves occur most commonly as responses to traumic and nutri-
tional stimuli (53, 54). An extensive examination of almost any pine
material, however, will reveal a few spontaneous simple leaves for the
transformation of which no known cause can be ascribed.
Fig. 4. — Dwarf shoots.
Six-needled dwarf shoot from P. C. Normal dwarf shoot from Ccdrus.
palustris. D. Abnormal dwarf shoot from P.
Normal three-needled dwarf shoot palustris.
from P. palustris.
During the first year of the present work several hundred buds were
removed from trees in the vicinity of Urbana, Illinois. The twigs from
which the terminal buds were removed usually responded in one of two
ways. They either pushed out and extended the units in the lateral buds
which ordinarily would have remained dormant, or they proliferated new-
branches from the old dwarf shoots (Fig. 3 A and B). Often new
branches came from both sources.
141]
EVOLUTION OF PINUS—DOAK
17
In those cases involving the forced extension of a dormant bud, the
subtending foliar components, which had for a time served as resting
primordia, seemed during this service to have had the future behavior of
their tissues fixed, because after extension these in all cases formed scales
Fig. S. — Proliferated dwarf shoot of P. pinaster.
A. Dwarf shoot. C. Simple green leaves with
B. Withered original leaves.
toothed margins.
of the usual type. As previously reported by Lloyd (53), those subtend-
ing structures which were deposited and extended during the same season
were, however, transformed into simple leaves (Fig 3 B and F and
Fig. 5 C). Those cases in which a proliferation grew from the old dwarf
shoots will be further described under the section dealing with the grow-
ing point.
It is a common observation that pines, when heavily fertilized, irri-
gated, or otherwise subjected to unusually favorable conditions, will pro-
18
ILUXOIS BIOLOGICAL MONOGRAl'llS
[142
duce simple leaves. Sometimes this occurs naturally (Biisgen, 17;
Goebel, 38), especially in southern climates. So frequently does it occur
in P. cubensis which grows on the Isle of Pines, surrounded as it is by
the warm waters of the Caribbean, that at one time efforts were made to
set up a new species (Rowlee, 74) based upon this character.
In certain conifers, notably Juniperus and Chamaecyparls, varieties
have been established which, when propagated vegetatively, maintain the
juvenile leaves throughout life. In horticultural literature these are
Fig. 6. — Twig from retinosporous pine (and miscellany).
A. The only fascicle on the twig. D. Winter bnd of P. palustris.
B. Simple subtending leaf. E. Scales from same showing inter-
C. Simple sterile leaves a part of which lacing fibers.
have been clipped away in order
to sbow the fascicle, A.
spoken of as retinosporous varieties. The attempt to obtain a pine with
simple leaves throughout has been only partly successful. It is not so
unusual, however, to find branches or entire young trees on which the
simple leaves predominate ( Fig. 6) . Several such trees are now growing
in the greenhouses at the University of Chicago while hundreds of such
branches may be found on trees growing at College Station, Texas.
Hochstetter (43) describes as "incomparably beautiful" a simple-leafed
variety of Pinus which he, for a time, was able to maintain but which
unfortunately perished after a few years.
143] EVOLUTION OF PINUS—DOAK 19
The wide differences between simple leaves in general and the foliar
organs now found on Pinus serve to emphasize the extreme foliar spe-
cializations of the genus. At the same time the simple leaves furnish us
with evidence regarding a type of leaf from which, or through which, the
numerous kinds of modern and highly specialized foliar organs of Pinus
have evolved.
B. Bud Scales, Sterile Bracts, and Subtending Scales
Of the eleven kinds of foliar components mentioned above, six are
scale-like. These are ( 1) bud scales, (2) sterile bracts of the main axis,
(3) fertile bracts of the main axis or subtending scales, (4) fascicle
sheath scales, (5) involucral bracts of the cones, and (6) cover scale or
bracts for the seed scales. The first three of these are found on the vege-
tative long shoot, while the involucral bracts, fascicle sheath scales, and
cover scales are borne on branches of a second order.
Like the simple leaves treated above, the scales on the main axis are
primary foliar organs. Of them Biisgen (17) says:
Observation and experiment alike teach that the bud-scales and leaves actually
originate in essentially similar rudiments whose later development is decided by
their surroundings, i.e., their relationship to other parts of the whole shoot com-
peting with them in growth and nutrition and to the climatic conditions.
As pointed out above the early removal of the leaves at the tip of a shoot
causes buds actually destined for development the following year to
extend in the year of their formation, and in this event true leaves are
formed from primordia which, in the ordinary course of things, would
have become scales.
This behavior is not surprising, for, as pointed out by Jeffrey (46)
and Fontaine (34), ancestral pines probably had simple leaves where we
now find the scale series and in addition bore fascicles similar to those
now found on pines. The transformed simple leaves, therefore, may be
looked upon as reversions.
The various kinds of scales present no fundamental morphological
differences. The units on which they are borne are here separated into
groups on the basis of (1) time of deposit, (2) amount of ultimate ex-
tension of the internodal component, and (3) presence or absence of
axillary components. Because of the morphological similarities through-
out the series, the description of bud scales which follows will, in most
respects, apply to all of the scales in the series.
Lewis and Dowding (SI) and others have given us works on the
anatomy and related phases of conifer bud morphology, but the best
modern summary of the literature dealing with the general subject was
given by Foster in 1928 (35). As early as 1880, however, Goebel (38)
called attention to the shortening of leaves and of internodes during the
20
ILLINOIS BIOLOGICAL MONOGRAPHS
[144
winter period of such scale-free conifers as Auracaria and Juniperus and
pointed out the fact that, even within a genus, we may have some forms
with bud scales and others without them, as in Podocarpus.
During the present work, the ontogeny of the scales was followed in
Piniis taeda L., P. palustris Mill., P. Laricio var. Austriaca End., P.
sylvestris L., and P. Pinaster Ait. The time of deposit and the time of
extension were observed. Since the putting down of new units is a
growth phenomenon, the deposit of primary foliar organs, when charted,
gives the typical S-shaped curve of growth (Fig. 30). The extremes are
marked by sterile scales, most of which are never separated widely from
each other and are, therefore, termed bud scales. Since, however, the
scales for a given year's growth are in two separated age groups, these
are for convenience termed, in the order of their deposit, "Group A" and
Fig. 7. — Miscellaneous.
Diagram of a longitudinal section
of a two-needled dwarf shoot
with normal interfoliar buds in
various degrees of development.
Camera lucida tracing of a trans-
verse section through the tip of
a winter bud of P. Laricio. The
black circles show the hooded na-
ture of the scales on the lateral
buds and fascicles.
C, D, E. F. Stages in the early develop-
ment of cotyledons, showing re-
duction in number of primordia
(after Buchholz).
G. Diagram of leaf orientation with
reference to axial plane (a, p)
in two-needled pines.
145]
EVOLUTION OF PINUS—DOAK
21
"Group B" (Fig. 2). Except for a difference in time sequence, the
ontogeny of the bud scales is similar in the two groups. "Group A" on
one year's deposit is in series proximally with "Group B" of the previous
year and distally with the sterile bracts of the main axis. The outer
scales in "Group A" become dry and frayed during their first growing
season. The scale blades become dead and scarious in their outer por-
tions but remain alive at their bases. A sharp line of demarcation sets off
living tissue from dead tissue (Fig. 2 H). The scales in "Group B"
spend the first winter as young tender scales or as meristematic primordia
(Fig. 2 G). During the second growing season these follow through
exactly the same ontogeny that has been described for "Group A."
Fig. 8. — Young bud scales of P. pin-
aster showing the early stages
of fraying.
Fig. 9. — Old scale from P. pinaster
showing method of fraying and in-
terlocked marginal fringes.
During the second summer while maturation processes are in prog-
ress, the origin of younger and more distal units (Fig. 1 K) slowly
crowds the scales in "Group B" to the base of the developing bud, where
they spend the second winter (Fig. 2 A). During the early spring of
their third growing season the covering of bud scales is ruptured, and the
scarious portions are either torn loose from the living base, as in the
forms with deciduous bud scales, such as P. sylvestris, or remain attached
as persistent bud scales, as in P. palustris.
The degree of bud scale specialization varies somewhat in the differ-
ent species. The most elaborate specializations occur in species with long
needles and persistent sheaths and are, therefore, well illustrated by P.
Fig. 10.— Fascicles and fascicle sheaths. (See explanation on opposite page.)
147] EVOLUTION OF PINUS—DOAK 23
palustris (Fig. 6 D and E) and P. Pinaster (Figs. 8 and 9). Here the
young bud scale, while still meristematic, forms a sort of hood (Fig. 11
B, C, and C) over the growing point of the stem and over all younger
foliar structures. "Group A" passes these stages rapidly while "Group
B" spends the first winter in the early stages of the process. Growth
goes on at a more rapid rate in tissues on the margins of the hood. At
this point the cellular orientation is such that, as the marginal cells
elongate, a sharp angle is made with those of the scale blade (Figs. 8, 9,
11, and 12). As maturation proceeds, these marginal cells elongate
enormously and become fibrous. The fibers are strong but are only
loosely bound together laterally, so that, upon the deposit and expansion
of the underlying structures, the resulting growth pressures rupture the
older and more mature scales according to a predetermined plan. This is
imposed by the nature and arrangement of the scale tissues and by the
sequence of growth processes within the scale itself (Figs. 8 and 9). The
angular arrangement and the fibrous nature of the tissues combine to
bring about the splitting of the blade and the fraying of the overhanging
hood-margin, especially along the line of angles where blade fibers and
marginal fibers meet. These processes continue until the hooded condi-
tion is no longer recognizable, each separate structure having been trans-
formed into a thin dry triangular scale with greatly frayed margin (Figs.
9 and 11 D). Upon the completion of these transformations the scale
series form numerous superimposed layers of papery wrapping around
the bud. The individual scales are interlocked by the tangle of tough
marginal fibers, and, if loosened at their bases, they may be unrolled from
the bud (Fig. 6 E) and still remain attached to each other. So tena-
ciously do they cling together that often a scale may be torn apart by
simply pulling on the attached neighboring scales. When in position on
the bud, considerable growth pressure is required to break these layers of
binding material. For this reason the interlocked scales often form bind-
ing rings (Fig. 13 e) or caps (Fig. 13 f) on partly developed shoots.
The angular margins, frayed edges, and strengthening effect of the
interlocking fibers were, in part, described by Lord Avebury (54), who,
however, did not describe the manner of their production. Fngelmann
(30) and Pilger (70) also describe the delicate interwoven fringes at the
Explanation of Fig. 10
A. Dwarf shoot of P. cembroides var. D. Same with sheath in act of shedding.
monophylla cut diagonally, with E, F, G. Old, middle-aged, and young
sheath in place at base of needle. fascicles of P. palustris, showing
B. Same with sheath removed, pulvi- progressive shortening of sheath
mis absent. by wrinkling.
C. Dwarf shoot of P. Ccmbra after H. Same as D.
shedding of the sheath, pulvinus
present.
24
ILLINOIS BIOLOGICAL MONOGRAPHS
[148
margins of the scales. Dufrenoy (26) figures a fringed scale (similar to
that shown in Fig. 11 D), and in describing his figure he says that the
scale leaf is "strikingly similar to scale of Cycas; the hairs may be in-
terpreted as sterilized ancestral ovules or stamens." The scale ontogeny
proves the incorrectness of Dufrenoy's interpretation, for the fibers at the
margins are neither hairs nor sterilized spore-bearing members but rather
the frayed blade margins of foliar organs.
Nearly all investigators who have worked with the bud scales of pines
are agreed that these scales exercise some sort of binding effect upon the
'mm^. Iff
Fig. 11.-
-Stages in hooding, fraying, and perforation
of bud scales and sheath scales.
A. Young scale primordium.
B. Hooded young scale with angular
marginal cells.
C and C. Perforation of bud scales
and sheath scales respectively.
D and D'. Mature bud scale and sheath
scale respectively.
E. Cellular detail along marginal angle.
F. Detail of overlapping fibers.
G. Diagram showing how overlapping
and angled margins permit ex-
pansion without disturbing the
binding efficiency of bud scales.
tissues within. This fact should be borne in mind, for this binding phe-
nomenon has probably had a part to play in leaf arrangement and in the
progressive reduction of the leaf number on the dwarf shoots which,
while young and plastic, are enclosed within the bud.
An exaggeration of the hooding phenomenon sometimes causes the
underlying growing point to push out through the crown of the hood
(Fig. 11 C and C), and, as the underlying parts are lifted up, an en-
149]
EVOLUTION OF PINUS—DOAK
25
circling sheath of fibers is left behind (Fig. 11 D') after the manner of
the orchrea in Polygonum. Hereafter this phenomenon is termed per-
foration.
The case of the scale on the long shoot is somewhat different, for,
subsequent to perforation, an increase in diameter of the encircled stem
soon ruptures the encircling fibers of the perforated scale. Perforated
blades and encircling fibers, therefore, represent but temporary stages in
Fig. 12. — Needle shapes (and miscellany).
a, b, c, d, and e. Camera lucida tracings
of transverse sections through
fascicles having one to five nee-
dles, respectively.
f. Theoretical diagram of six-needled
fascicle.
g. Outline of a section through a ten-
needled dwarf shoot showing
two whorls of five needles (after
Schneider).
h to o. Semi-diagrammatic drawing of
fascicle scale series at the time
of perforation.
hh. Lateral scales.
i. Central scale with frayed margin.
j to 1. Perforated scales.
m and n. Hooded scales.
-'<>
ILLINOIS BIOLOGICAL MONOGRAPHS
[150
bud scale ontogeny (Fig. 11 C and D). The insignificant increase in
diameter of the dwarf shoot permits the perforated scales on it
to remain as a more or less permanent encircling sheath (Fig. 11 C and
e
Fig. 13. — Young long shoots of P. sylvestris. (See explanation on opposite page.)
151] EVOLUTION OF PINUS—DOAK 27
D') through which, by basal growth, the needles are forced as through a
cylindrical die. As hinted by Eichler (29), it is this die-like action which
gives the needles their characteristic cross-sectional forms (see Schneider,
79).
Except for a difference in the amount of extension undergone by the
corresponding internodal components, the sterile bracts are in every way
similar to the bud scales in "Group A" with which they are in direct
series on the distal side.
On very vigorous shoots each year's growth usually has a number of
units with extended internodal components but which are devoid of axil-
lary buds (Fig. 13 b and Fig. 14 d to e). The sterile bracts or foliar
components of these units lie between the last true bud scales and the first
subtending bract. They usually remain in the bud for only a single
winter. At extension of the main axis, the scarious portion is often lost
and the living base alone remains. This remnant we may think of as a
leaf scar or leaf cushion.
The line of demarcation between sterile bracts and the true bud scales
is not a clearly defined one. After extension, the bud scales continue to
occupy their crowded position at the base of the year's growth or, when
shed, leave a ring of crowded scars to mark the points from which they
have fallen (Fig. 3 m and n), thus dividing the twig into a series of easily
recognizable annual growth segments (Fig. 15). The sterile bracts or
bract scars do not remain crowded but at extension come to occupy rela-
tively wide intervals along the base of the year's growth (Fig. 14 d to e),
for at this time the two types of scales are similar and lie in continuous
series at the base of the winter bud (Fig. 2 A and B). One cannot
determine exactly what fractional part of the sterile scale series at the
base of a dormant bud belongs to each of the two types. An approxi-
mation can be made, however, by counting the scars left on the same twig
in previous years. This is made easy by the fact that most pines leave
an indelible record of the various units produced on each year's growth
long after their foliar components have disappeared (Fig. 3 E). In some
cases the units produced in any given year can be counted with certainty
Explanation of Fig. 13
L. Vigorous shoot with laterals. N. Long shoot with young and one-
a. Lateral long shoots develop- year cones and normal laterals.
ing one season in advance c'. Young ovulate cones,
of the usual time. d. One-year ovulate cone.
b. Naked base covered with ster- g. Normal lateral long shoot.
ile bract scars. O. Branch with binding ring of bud
M. Sectioned tip showing ovulate scales.
cones. e. Binding ring.
c. Ovulate cones. P. Long shoot with staminate cones.
f. Binding cap of scales.
28
ILLINOIS BIOLOGICAL MONOGRAPHS
[152
Fig. 14. — Young long shoots of P. tonyosho. The left branch is normal. The
right branch has the staminate cone series interrupted by bisporangiate cones.
(See explanation on opposite page.)
153] EVOLUTION OF PINUS—DOAK 29
for periods in excess of a quarter of a century (Fig. 15). After the
counts are made and averages taken, one may divide the total bud units
in the sterile series of the dormant bud into two approximately correct
groups, using for this purpose the average percentages of scales and of
sterile bracts produced by the same twig in previous years.
At its distal end, the sterile bract series is continuous with the stami-
nate cone series (Fig. 14) ; but if, as is often the case, the latter is
omitted, then direct contact is made with the dwarf shoot series (Fig. 13
L and N). The first fertile scale in either orthostich or parastich usually
marks the beginning of the fertile series, which, from that point to its
end, remains unbroken. This is not always the case, however, for stam-
inate cones may intrude themselves into the dwarf shoot series or vice
versa.
A similar overlapping is found between sterile bracts and cones and
also between sterile units and fascicled units. These interruptions are not
always confined to the borderline between series. In P. palustris, and
less frequently in other species, interruptions by the intrusion of one or
several units of a different type occur well up in the body of a series.
This is especially true of the intrusion of sterile units into the dwarf
shoot series. Such gaps occur most frequently on the ventral surface of
horizontal twigs (Fig. 16 A). Gaps in the various fertile series are espe-
cially frequent on those twigs on which the scale leaves have been re-
placed by simple leaves (Fig. 5).
The fertile units of a given year's growth, save for the presence of
axillary outgrowths, are similar in every way to the extended sterile units
described above ; and the accompanying scales are in even- detail like
those already described.
Before leaving the general subject of scales, it is probably worth while
to restate the chief points in regard to these organs. It seems certain
that regardless of type the scales have developed from leaves of a simple
nature. The main peculiarities of pine scales, in comparison with the
scales of other plants, are bound up with the phenomena of hooding,
fraying, and perforation, the results of which permit the scales to exert
binding pressures upon the organs growing within them. Pinus is also
peculiar in that all the primary foliar organs are normally scale-like.
Explanation of Fig. 14
atob. Normal ovulate cone. xx. Bisporangiate cones in staminate
btoc. Dwarf shoot series. cone series,
ctod. Staminate cone series. d to e. Sterile bract series.
f. Bud scale scar.
30
ILLINOIS BIOLOGICAL MONOGRAPHS
[154
ABC
Fig. IS. — Twigs of P. Laricio from the north (Illinois) and of P. palustris
from the south (Texas) with dated annual growth nodes.
A, Twig of P. Laricio, normal except
for 1929, a year in which the ter-
minal bud was destroyed. Sub-
sequent growth came from a lat-
eral bud.
B. Twig of P. Laricio, normal except
for shortening of internodes and
leaves of 1930 due to transplan-
tation of the mature tree in the
winter of 1929.
C. Normal twig of P. Laricio.
D and E. Stripped twigs of P. palus-
tris showing multinodal growth
for 1931.
155] EVOLUTION OF PINUS—DOAK 31
C. Homologies of the Axillary Shoots
Turning now from the foliar to the axillary components on the vege-
tative long shoot, we find these to be of four types, viz., staminate cones,
dwarf shoots, branch buds, and ovulate cones. The staminate cones and
dwarf shoots fall naturally together in one group, and the branch buds
and ovulate cones comprise another.
The staminate cones and dwarf shoots are alike in origin and in posi-
tion. They have determinate growth and are deciduous. Each is clothed
at the base with a series of thin scales. Without a clear borderline
between them, the cone and dwarf shoot series lead directly into each
other. These facts make it clear that in Pinus the axis of the staminate
cone and that of the dwarf shoot are of the same order and are as nearly
homologous as it is possible for fertile and vegetative shoots to be.
Near the end of a year's growth and terminating the orthostiches of
fertile units on the long shoot, one to several branch buds occur. These
usually deposit their basal scales during their first season (Fig. 2 E).
The fertile units for their first year's growth are deposited during the
second season, and extension of their first year's growth occurs during
the third season (Fig. 13 g). On vigorous shoots this program can be
shortened (Fig. 13 a), in which case the lateral long shoots are seen as
lateral extensions of the year's growth upon which they are borne. In
this position they are strikingly suggestive of young ovulate cones which
not only occupy similar positions (Fig. 13 a and c) but originate at the
same time in the ontogeny of the year's growth. The presence of sec-
ondary dwarf shoots (brachyblasts or seed scales) upon their axes mark
the cones as modified long shoots, as does also the frequent proliferation
of their growing points into long shoots. These evidences make it clear
that the ovulate cones and the lateral long shoots are of the same order
and that the ovulate cone, therefore, should be looked upon as a modified
long shoot.
D. Normal Annual Growth of the Vegetative Long Shoot
Without attempting to analyze the complex of physiological conditions
upon which the regular sequence of events within a pine bud is depend-
ent, the story of seasonal bud behavior is briefly outlined below:
Upon the return of favorable growing temperatures following the
winter rest, the intcrnodal tissues of the bud units ( Fig. 2) are first to
spring into vigorous activity. Although the other parts (dwarf shoots,
sheath scales, needles, etc.) seem ready to grow, something seems to
inhibit them. Only the cones are able to compete with the internodal cells
as the latter enter actively into their long delayed grand period.
Fig. 16. — Stripped twigs showing annual growth nodes
A. Ventral surface of a twig of P. pa-
lustris. Inked circles show blanks
in the dwarf shoot series. The
series was continuous on the dor-
sal side.
B. Twig of a white pine from Massa-
chusetts.
C and D. Multinodal twigs of P. palus-
tris from Texas. The numbered
segments represent successive
fertile series deposited during the
years indicated.
157] EVOLUTION OF PINUS—DOAK 33
As the internodal tissues pass the crest of their grand period and
begin maturation, the tissues of the dwarf shoots and of their foliar
organs (sheath scales and needles) spring into vigorous activity. These,
as pointed out by Kiister (49), all spend the winter in approximately the
same developmental stage. As the outermost scales of the sheath begin
to mature, the needles in their turn become the conspicuous extension
organs. Their growth is accelerated for a time, but, as the summer ap-
proaches, it becomes slower and more irregular.
Soon the distal portions of the scales and leaves become matured and
growth becomes confined to narrow basal zones. While active growth is
still in progress, the matured portions probably carry on their full share
of photosynthetic and protective work respectively. While leaf, scale, and
cambial growth are still active, the deposit of new units is begun at the
growing point of the long shoot. This manifests itself first by a slow
addition to the sterile primordia already present at the tip of the axis
("Group B" of previous season). As the growth processes become more
rapid, fertile units are deposited (Fig. 1 K). On slowly growing twigs
the fertile series usually begins with pollen cones followed by short
shoots. The cones may, however, fail entirely. On vigorous twigs pollen
cones are seldom deposited, and in this event the first units in the fertile
series are dwarf shoots.
The time sequence for both deposit and extension is somewhat vari-
able, depending upon the species, the latitude, and the season. The dif-
ferent species in a given locality start activity at approximately the same
time and at first run parallel courses. As summer progresses, the species
which mature their needles early (usually those with short needles) ad-
vance more rapidly and begin the deposit of new units, while the species
with long needles are continuing the growth of these organs. As fall
approaches, however, the species with long leaves and a proportionately
greater photosynthetic area are accelerated in their processes ; and, by the
onset of the winter rest, all have attained corresponding growth stages.
E. Abnormal Annual Growth of the Long Shoot
1. Multinodal Annual Growth and Summer Shoots
In case the season of deposit is interrupted by a hot dry period fol-
lowed later by rains and a return of favorable conditions, a so-called
multinodal year's growth is produced. These multinodal shoots are es-
pecially frequent in southern pines and are more likely to occur in some
species than in others. This behavior was observed most commonly in
P. palustris growing at College Station, Texas. Indeed, multinodal
growth in this case was more the rule than the exception (Fig. 16 A,
C, andD).
.51
ILLINOIS BIOLOGICAL MONOGRAPHS
[158
It was found that by stripping the bark from a year's growth the
separate series of fertile units could be displayed to good advantage. This
is made possible by the fact that those portions of the wood from which
sterile bracts are stripped appear smooth. The woody cylinders leading
to the dwarf shoots, however, clearly mark the points from which these
structures grew (Fig. 20 D and E).
KHi
Fig. 17. — Two sets of mature cones of P. taeda produced in the
same season as a result of multinodal growth.
In each case of multinodal growth, as conditions become unfavorable,
the twig behaves exactly as if ceasing deposit for the year. The dwarf
shoot series gives way r to the usual number of lateral buds (and ovulate
cones, if these are to be produced), after which the regular series of
scales ("Group B") is deposited. When favorable conditions return, the
dwarf shoot series is resumed and continued until again brought to a
similar close. This process may be repeated a second or even a third time
in a single summer ( Fig. 16 C and D).
159] EVOLUTION OF PINUS—DOAK 35
Multinodal shoots are related to the so-called summer shoots which
sometimes result when the season is unusually long and the break be-
tween favorable seasons is marked. In this case the units which are
deposited in the early period may be extended in the fall or late summer
of the same year in which they were deposited. This occurred on many
twigs of P. palustris and P. pinaster at College Station, Texas, in the
summer of 1932.
2. Lateral Cones
If, as pointed out by Shaw (82), the multinodal twig under considera-
tion is producing ovulate cones, those that close the first fertile series will
be in the so-called lateral position, while those closing the last series will
appear to be either terminal or sub-terminal. Actual terminal cones are
extremely rare. Masters (57) says that they are never really terminal.
Cases of actual terminal cones are on record, however, these having been
described by Tubeuf (93) and Worsdell (104).
The production of two to several sets of cones on the same year's
growth is common as shown by Mayer (59) and Gates {2>7). In the
course of the present work numerous cases of this type were found, most
of which occurred on trees from stations in Texas. Figure 17 shows
such a specimen which produced, at the upper end of the first fertile
series, a set of four cones and several branch buds. These were followed
by numerous sterile scales and finally by a second series of dwarf shoots
which again was terminated by four cones, making a total of eight, four
of which were in the lateral position and four in the so-called terminal
position. Each set of these cones occupied the same relative position with
reference to a fertile series of units, the nature and order of which was
determined by external conditions. As pointed out by Mayer (59), the
so-called lateral cone, in the light of these observations, becomes a matter
of ecologic interest rather than a fixed taxonomic character.
3. Intrusion of Ovulate Cones into
Staminate Cone Series
Several young trees of P. tonyosho were observed in which ovulate
cones had partly or completely replaced the staminate cones. These trees
produced, in what ordinarily would have been the pollen cone series,
staminate cones at the base, bisporangiate cones* in the middle, and
ovulate cones at the top (Fig. 14 x). The plants which produced this
curious arrangement grew as a border planting and had evidently been
heavily fertilized. A somewhat similar grouping of cones has been re-
ported by Fujii (36), who says that up to a certain stage the cones may
*Of these cones more will be said in the section dealing with the seed scale, where their
transitional scales will be discussed.
36
ILLINOIS BIOLOGICAL MONOGRAPHS
[160
Fig. 18. — Abnormal long shoot and dwarf shoot of P. pinaster.
A. Long shoot with dwarf shoots in B. Dwarf shoots from A, showing
place.
over-developed interfoliar buds
and the relation of leaf length
to bud size.
161] EVOLUTION OF PINUS—DOAK 37
be developed into pollen or ovulate types, depending upon nutritional con-
ditions. Similar bisporangiate cones have been reported by Righter (73)
and by Meehan (60). The latter has even proposed a "law of sexuality"
for the conifers, in which he holds that the "sex" is determined by the
vigor of the twig upon which the cones are borne.
The replacement of other fertile units by ovulate cones expresses itself
variously (Fig. 19 D). Sometimes the physiological condition is such that
all the axillary outgrowths are replaced by ovulate cones. This condition
has been reported by Keslercanek (48), Mullins (63), Witmack (103),
Tubeuf (94), and others. As many as ninety-six ovulate cones have been
found in series on a single twig.
4. Abnormal Axillary Bud Development
Another case of abnormal annual growth involved several twigs of
P. pinaster growing at College Station, Texas. For some reason the
growth of dwarf shoots on these did not stop at the customary point but
proceeded in each case to make a long dormant bud (Fig. 18). Since
these abnormal short shoots were borne at all axils, the long shoot,
although little modified, may be looked upon as being abnormal in its
secondary product. A similar twig has been reported for Abies by
Tubeuf (94), who states that they are of frequent occurrence in this
genus. This observation is interesting in that it is suggestive of a latent
ability of Abies to produce branches in the axils of all its leaves. This
suggestion is further strengthened by the fact that members of this genus
often produce dwarf shoots as shown by Masters (57), or proliferate the
seed scales into shoots as shown by Stenzel (86) and others:
III. THE REPRODUCTIVE LONG SHOOT, OR
OVULATE CONE AXIS
A. Primary Foliar Organs
Near the point of attachment to the main axis, the ovulate cone
produces several sterile units which bear scale-like foliar components, or
involucral bracts (Fig. 1 H 2 ). Morphologically these are very similar to
the scales already described for the main axis. They are broader, how-
ever, less frayed at the margins, and are probably never perforated.
Higher up on the cone, fertile units are borne. The axillary com-
ponent of each fertile unit is the much-discussed seminiferous scale.
The primary foliar component of these fertile units is the cover scale
(Fig. 1 C 5 ). In the pines it remains small and woody and is sometimes
partly fused against the seed scale. That these structures are indeed leaves,
38
ILLINOIS BIOLOGICAL MONOGRAPHS
[162
~>%
S^
^iflM-Ses
-*Sl
<&*," »
"'iff*
£
Fig. 19. — Miscellaneous. (See explanation on opposite page.)
163] EVOLUTION OF PINUS—DOAK 39
at least in Abies, has been shown by Willkomm (102). In Lar'ix, as was
pointed out by Masters, they grow into functional leaves (Fig. 24 G).
As shown by Aase (1), the vascular strands from the cone axis to
the bract and seed scale vary somewhat, depending upon whether one ex-
amines the tip, the middle, or the base of the cone. The middle or func-
tional region tends, however, to give off bundles to bract and seed scale
exactly as the vegetative long shoot gives off bundles to the subtending
scale and the short shoot (Fig. 23 A and J).
B. Growing Point
On the cone axis the tip meristem usually is transformed entirely into
woody vestiges which give no evidence of an earlier latent ability to con-
tinue into foliage-bearing branches. However, as shown by Masters (57),
Thiselton (89), Stenzel (86), Willkomm (102), Tubeuf (95), and others,
and as I have observed in several relatives of Pinns, indeterminate growth
of the cone axis is not uncommon. Masters (55) and others have de-
scribed proliferated cones in Larix, a genus in which these cones seem to
occur most frequently. During the present work several such cones were
found growing on Larix europea at Urbana, Illinois. Coulter and Cham-
berlain (22, p. 414) express the opinion that certain gymnosperms, like
Torreya, have evolved beyond the stage of the compound strobilus by
simply proliferating the cone axes and then transforming all the scales,
save one, into leafy shoots.
Certain proliferated cones of Abies which were described by Will-
komm (102) so closely resembled the precociously proliferated branch of
Pinus pinaster (Fig. 18) described above, that for comparative purposes
a few of Willkomm's figures are here reproduced (Fig. 29 z and z' ;
Fig. 32, parts 7, 8, and 9). A comparison of these figures will reveal
the fact that the subtending scale of the pine shoot has its counterpart
in the leaf-like cover scale on the Abies twig. The lateral scales on the
dwarf shoot of the pine twig (Fig. 25 C) correspond in position to the
leaf-like lateral expansions (megasporophylls) on the secondary shoots
of the proliferated Abies cone. The tip buds of the two are, of course,
homologous ; and no doubt the fascicle sheath scales and needles which
Explanation of Fig. 19
AandC. Needles from bound fascicles D. Staminate cone series of P. tonyo-
of P. palustris. sho largely replaced by ovulate
B. Abnormal shoot of P. pinaster with cones.
simple leaves and staminate E. Bud of P. Laricio with one fascicle
cones. developing one season in advance
of its normal time.
F. Bisporangiate cones of P. tonyosho.
40
ILLINOIS BIOLOGICAL MONOGRAPHS
[164
Fig. 20.— Comparative studies of the woody cylinders
of Taxodium distichum and Pinus palustris.
Stripped twig of Taxodium show- D. Stripped twig of Pinus with the
ing the projecting ends of woody cylinders of the dwarf
branched dwarf shoots. shoots projecting.
Same with surface layers removed. E. Same but older.
Same in radial section. F. Same in radial section.
165]
EVOLUTION OF PINUS—DOAK
II
cover the bud in Pinus find their counterparts in the basal scales which
cover the bud of Abies.
When it is remembered that the abietineous cone is a conservative
structure and that the pine twig just described is only an exaggerated
phase of a condition which occurs normally in this genus, one is im-
pressed with the probability that some ancestor of Abies had dwarf
shoots and that the present form of the genus has been attained by sec-
ondary loss of these structures. This view is further strengthened by the
observations of Tubeuf (94) who found occasional vegetative twigs of
Abies with buds in the axils of all their leaves.
Fig. 21.— Diagrammatic drawing of the imbedded dwarf shoot of Taxodium
distichum, showing the relation to successive deciduous shoots.
The tip meristem of another cone described by Willkomm had pro-
liferated a long branch of ordinary vegetative type, the lower one-third
of which had produced some axillary tissues corresponding in position
and texture to the seed scales with which they were in series. These
tissues filled up the space between the subtending leaf and the main axis,
thus making the base of the latter concrescent (Fig. 29 x and x'). Since
the seed scale is a dwarf shoot, this evidence suggests the possibility that
the origin of concrescent leaves in conifers was associated with the dis-
appearance of dwarf shoots from their axils.
In summary it may be said that exceptions to the rule of determinate
growth of cones occur with sufficient frequence to convince us of their
latent power of becoming indeterminate. The nature of these exceptions
shows clearly that the megasporangiate strobilus is a compound struc-
ture and, therefore, its axis is equivalent to a long shoot and its scales
are equivalent to dwarf shoots.
42 ILLINOIS BIOLOGICAL MONOGRAPHS [166
IV. THE EVOLUTION OF THE LONG SHOOT
A. The Vegetative Long Shoot and Its Foliar Organs
If we may assume that some remote macrophyllous ancestor of Pinus
was devoid of resting buds and had both monomorphic branches and
monomorphic leaves with no delay between deposit and extension
(Fig. 29 a), then the steps in the evolution of the long shoot of Pinus
with its characteristic, scale-like, primary leaves, its compound bud, and
its well-marked annular growth-nodes, would seem to have been as
follows:
1. Adaptation to temperate climates with seasonal climatic changes
required protection of the meristematic tips. The plant met this need by a
delay in the onset of the grand period of growth, thus bringing more and
more foliar organs to overlap and protect the growing point.
2. The recurring need for protection during certain seasons (winter
or drought) alternated with seasons of active vegetative growth and thus
tended to fix the protective function on certain of the leaves on the long
axis. These became specialized in this work and were transformed into
scales. The remaining leaves on the long axis remained crowded within
the scaly cover during unfavorable conditions and were later extended as
food makers. The scales with their protected content of embryonic units
thus formed a simple bud (Fig. 29 c and d).
3. A still further delay, both in the time of deposit of units of the
main axis and the time of extension, led to a further telescoping of parts
until all the primary leaves became scale-like ; and the rudiments for the
lateral units were produced before leaving the bud, thus leading to the
formation of the compound bud (Fig. 2) which limited and shaped the
growth of the enclosed short shoots.
4. The periodic extension of the compound buds gave rise to the
characteristic annual growth nodes of the long shoot (Fig. IS) as already
described.
B. The Ovulate Long Shoot, or Cone Axis
That the steps leading to the compound ovulate strobilus closely paral-
leled those leading to the formation of the compound winter bud is at-
tested, first, by similar vascular units (Figs. 23 A and H) and, secondly,
by the same arguments which were used earlier in this paper to support
the homology of lateral long shoots and ovulate cone axes. The cogent
fact that their secondary outgrowths (dwarf shoots and cone scales)
run such close parallels is also suggestive of a parallel in the evolution of
the long shoot and the cone axis.
The steps leading to the compound strobilus were taken at a time
when the ancestors of Pinus were perhaps at the Cordaitean level. So re-
167]
EVOLUTION OF PINUS—DOAK
43
mote was that period that little fossil evidence of the course of this evo-
lution has as yet been found. If the supposed parallel between vegetative
and fertile long shoots is an actual one, then the compound strobilus
must have resulted from internodal shortening of a fertile long shoot
which bore numerous simple fertile shoots at its nodes. In a manner
analogous to that by which numerous dwarf shoots were brought together
to form the compound bud, this shortening brought together the numer-
ous simple strobili, or primitive seed scales (Fig. 32, parts 1, 2, and 3)
into a compound strobilus. Just as pressures within the compound bud
limited, shaped, and displaced the sheath scales of the dwarf shoot, so
the formation of the compound strobilus limited, shaped, and displaced
the sporophylls on the simple strobili.
V. THE VEGETATIVE DWARF SHOOT AND
ITS FOLIAR ORGANS
Turning now from the cone and the more or less generalized long
shoot to a consideration of the shortened and highly specialized dwarf
shoot, we find that its primordium is put down in the axil of the scale
Fig. 22. — Diagrams showing corresponding structures as they appear during
the development of the dwarf shoot and seed scale of Pinus.
A to E. Stages in the development of the dwarf shoot and its vascular supply.
F to J. Corresponding stages in the development of the seed scale.
SS. Subtending scale. CS. Cover scale.
GP. Growing point. CSc. Central scale.
L. Leaf. CSp. Central sporophyll.
LS. Lateral scale.
II
ILLINOIS BIOLOGICAL MONOGRAPHS
[168
Fie. 23. — Diagrams of vascular structures showing the writer's views with
reference to the relationships existing between the dwarf shoot of Pinus, the cone
scale of Pinus, and the cone scale of Araucaria.
A. Supply to dwarf shoot and subtending scale of P. Banksiana (redrawn from
Aase).
B. Same as A, but with supply to sheath scales and needles added.
C and D. Transverse sections through vascular supply to three-needled dwarf
shoot. The bundles to the lateral scales and the central scale are exaggerated
for emphasis. {Continued on opposite page.)
169] EVOLUTION OF PINUS—DOAK 45
primordium in mid-summer (Fig. 1 K and Fig. 30). The young dwarf
shoot primordium gains rapidly the rudiments for all its sheath scales and
for its functional leaves as was shown earlier. All these structures are
extended during the season following their deposit.
A. Sheath Scales
1. Morphology
In all pines examined, the three most proximal of the foliar organs on
the dwarf shoot were regularly and definitely placed with reference to
the axes of both the long and dwarf shoots. The first two were always
on opposite sides of a plane passed through the long axes of both the
dwarf shoot and the long shoot (Fig. 1 N and Fig. 25 C), and the third
was directly between the two axes and was bisected by their common
plane. Hereafter in this paper this plane will be spoken of as the axial
plane; the first two scales on the dwarf shoot will be called the lateral
scales; the third scale will be termed the central scale.
The lateral scales are opposite each other, thickened at the base,
keeled, and exhibit little or no intercalary growth. They are seldom per-
forated but are often serrate on the keel, and in other characters they
are set off sharply from the papery sheath scales which follow them
(Fig. 22 D and Fig. 12 hh).
Granting that the two lateral scales represent successive foliar organs
on the dwarf shoot, it follows that the internode between them has been
lost and that the scales have been displaced from their phyllotaxic po-
sitions. This view is supported by the fact that if we begin far enough
Explanation of Fig. 23 {Continued)
E. Supply to five-needled fascicle showing in dashed lines the location of the
supply to the inner circle needles when present (drawn from Schneider's
description).
F. Supply to two-needled fascicle.
G. Supply to the one-needled fascicle showing vestige of bundle to the aborted leaf
as found in monophylla (from Schneider's description).
H. Supply to typical cone scale and bract (modified from Aase's drawing of P.
maritima) ,
I and J. Transverse sections through // at different levels (redrawn from Aase).
K. Diagram of final distribution of the four bundles seen in /.
L. Diagram of supply to lowest scales and bracts on typical cones of Pinus (re-
drawn from Aase's figure of P. Banksiana) .
M, N, O, and P. (Redrawn from Aase's figures of P. Banksiana) .
Q, R, and S. Supply to scale of Araucaria Balansi (modified from Aase).
T. Diagram of principal bundles in scale of Araucaria.
U. Subdivision of bundles in sterile scale of A. Balansi (modified from Aase;
dashed lines separating branches of principal bundles supplied from her des-
cription).
V. Diagram of a cross section of Agathis vitiensis (modified from Eames).
W. Diagram of ramifications of bundles in scale of Araucaria.
-16
ILLINOIS BIOLOGICAL MONOGRAPHS
[17H
— I
A
B
f
D
Fig. 24. — Dwarf shoots of Larix and Ginkgo.
(See explanation on opposite page.)
171] EVOLUTION OF PINUS—DOAK 47
distally on the dwarf shoot, the angle between successive foliar organs
regularly conforms to a two-fifths phyllotaxy ; but, as the lateral scales are
approached, the displacement becomes evident (see arrows in Fig. 25 C).
The central scale is displaced to a less degree and more closely re-
sembles in form and texture the regular sheath scales. The differences
separating it from the other scales would perhaps not justify the assign-
ment of a special name to it, but, as will be shown later, the central scale
has had a homologue in the evolution of the sporophylls to form the
cone scale and demands, therefore, both a special name and special notice.
In addition to the lateral scales and the central scale, there is deposited
on the young dwarf shoot a series of scale primordia which show little
or no displacement. These are the regular fascicle sheath scales.
All the scales spend the winter in the meristematic condition
(Fig. 25 F).
Spring growth (extension) begins almost simultaneously in all of
these young scales, but maturation is in acropetal succession. This re-
sults in a constantly increasing length of scale from the proximal to the
distal end of the fascicle scale series (Fig. 12 h to o).
In their later ontogeny, the scales follow through the processes of
hooding, fraying, and perforation as described for the bud scales earlier
in this paper. Here, however, these processes, especially perforation and
the reverse growth of the marginal cells, are far more pronounced than
in the bud scales already described. The situation is complicated still
further by the development of intercalary meristems at the bases of the
sheath scales by which these continue growth after perforation has been
accomplished. Because the dwarf shoot undergoes such limited secondary
increase in thickness, the sheath ordinarily encircles the base of the
needles from which the scales may be slipped off one by one without
being split.
With several superimposed layers of papery scales overlapping them
and hindering their elongation, it is not surprising that pine leaves have
developed needle-like points for perforating these layers. There is ob-
viously a close correlation between the complexity of the sheath and the
Explanation of Fig. 24
A. Twig of Larix europea. C. Normal Ginkgo twig showing wide
x. A dwarf shoot which later ex- interval between successive dwarf
tended to make a long shoot. shoots.
B. Long shoot of Ginkgo. z. Bud scale scar.
y. A portion of the long shoot D. Same as A.
failed to extend, thereby E and F. Larix twigs with repeatedly
making a dwarf shoot. branched dwarf shoots.
G. Larix cone growing from one mem-
ber of a four-parted dwarf shoot.
48
ILLINOIS BIOLOGICAL MONOGRAPHS
[172
Fig. 25. — Comparative studies of the early development of leaves
in P. cembroides var. monophylla and P. Laricio.
A. Camera lucida drawing of a longitudinal section of the leaves of P. cembroides
var. monophylla soon after the beginning of spring growth.
B. The same less highly magnified and showing the hooded scales and other related
structures.
C. Camera lucida tracing of a transverse section through the developing fascicle
of P. cembroides var. monophylla showing the rudimentary second leaf, the
phyllotaxy, and the displacement of the lateral scales.
D and E. Cross sections of dwarf shoots from P. cembroides var. monophylla and
P. Laricio at stages corresponding to B and F, respectively.
F. Longitudinal section of winter dwarf shoot of monophylla.
G. Longitudinal section through young leaves of P. Laricio in a stage of develop-
ment comparable to that shown for monophylla in B.
H. Diagram of imbedded winter bud of Taxodium disticluim.
I. Double leaf primordia of P. cembroides var. monophylla in winter condition.
173] EVOLUTION OF PINUS—DOAK 49
development of horny and otherwise highly specialized points on the
needles of Pinus.
Meehan (61) speaks of a "membrane" on P. monophylla which he
says is present at the beginning of needle growth. By releasing this mem-
brane Meehan thought that he could influence the number of needles on
the dwarf shoot. Without doubt the structure referred to was nothing
more than the multiple cover of sheath scales.
Collectively, the scales form a binding sheath for the fascicle of
leaves. By reenforcing the point made weak by the basal meristems, the
sheath makes possible the long-continued growth of the needles. In this
respect the fascicle sheath is analogous to the encircling leaf sheath of the
grasses.
The effectiveness of the sheath as a strengthening splint may be easily
demonstrated by simply removing it from fascicles on which the leaves
are actively growing. In this case the leaves fall limp, hang in a pendu-
lous fashion, become dried at the base, and soon break off. The drying
gives evidence of a secondary function of the sheath, i.e., the prevention
of excess evaporation from the young parts which are as yet unprotected
by a cuticle.
Once the needles are mature, the zonal meristems are lost. Mechani-
cal and epidermal tissues are formed for parts within the sheath, and
consequently its strengthening function is no longer required. This is
evidenced by the fact that in many pines the sheaths are deciduous, fall-
ing away at the maturation of the leaf bases or soon afterward. Indeed
the fascicle sheath, by obstructing the light from the basal portion of the
leaf, becomes positively detrimental in that it appreciably reduces the
photosynthetic area of the leaves.
2. Methods of Scale Removal
Pines have evolved several mechanisms for removing this obstruction.
In some species the fascicle scales are more or less stiff and are weakly
attached at their bases and have only a few of their distal scales per-
forated. As long as the needles are growing rapidly, the tissues within
the encircling fibers are in the first phase of growth. The cells of such
tissues are small, and consequently the total diameter of the encircled
leaves is small. As elongation slows down and the maturation zone
reaches points nearer and nearer the base, there comes a time when the
enlarging basal portions of the leaves expand within the encircling fibers
until the jacketing sheath is broken apart. Near the basal point of attach-
ment an absciss layer is now formed from which the scales are soon
broken by the movement of the leaves in the wind. The scales leave a
bulging cushion or scar at points from which they fall away. When the
50 ILLINOIS BIOLOGICAL MONOGRAPHS [174
scales have been shed, the needles are left exposed to the light and air
for their full length.
In P. excelsa, P. flexlis, and many others the scales are stiff and
weakly attached at the base as described above, but the few perforated
scales are more or less proximal in position. In this case the functional
leaves, when mature, develop a special basal enlargement (Fig. 10 C and
Fig. 1 L and M) which breaks the encircling fibers. The expansion of
these structures forces the scales sharply outward and breaks them off,
leaving the mature dwarf shoot entirely free of scales (Fig. 10 D, H,
and C).
A third method of ridding the fascicle of its scaly sheath is found
in P. cembroidcs in which the scales and leaves mature simultaneously.
After maturation the former become brittle and dry. Upon drying, they
warp and break and thereby eocpose the leaf base to the light. Since the
breaking is not at a predetermined point, a ragged rosette of papery
scale bases is left. These remnants become smaller and smaller until after
a time their obstruction to light and gases is negligible (Fig. 10 A).
As a rule the pines with persistent sheaths have more scales, and these
are perforated to a far greater extent than is the case in pines with
deciduous sheaths (Fig. 10 F, F, and G). As the enclosed portions of
the needles mature, the encircling scales are frayed sufficiently to ac-
commodate the increased diameter of needles ; and the sheath, although
remaining unbroken (Fig. 11 D'), is shortened until finally two-thirds or
three-fourths of the originally covered portion of the leaves lies exposed.
3. Scale Number per Dwarf Shoot
In view of the possibility that the fascicle scales for the various
species of pines would show numerical differences, as had been found
by Engelmann (30) for the involucral scales at the base of the staminate
cone, scales from the fascicles of each species and variety studied by the
writer were counted and tabulated (Table 1). The extreme range is
from seven, a minimum for P. albicaulis, to twenty-three, a maximum for
P. Torreyana. The widest range in any one species is found in P. palus-
tris, which, because of the uniformity in samples taken from several
trees growing at College Station, Texas, was selected for testing the
variation in scale number from place to place over the geographic range
of a species. Samples taken from each of nine stations show that, on the
whole, the numbers are related ; but the samples taken from College
Station, Texas, are far higher. Those samples from Foxley, Alabama,
however, are lower than was anticipated. The cause of this wide varia-
tion may be due either to climatic conditions or to varietal differences
within the species.
175] EVOLUTION OF PINUS—DOAK 51
The widest range found among the fascicles of a single tree was in
P. rigida, on which there seemed to be a difference in the scale number in
fascicles taken from the various parts of a year's growth. This was ob-
served also in a sample of P. palustris from Beaumont, Texas. The latter
specimen had a summer shoot, and the fascicles which grew on this had
a scale number which was less than that for the fascicles on the regular
year's growth.
In order to test the variation in the scale number with reference to
the position of the fascicles on the year's growth, vigorous twigs of
P. pinaster, with a minimum of thirty fascicles on each year's growth,
were selected; and ten fascicles from base, middle, and top, respectively,
were removed and the scale number counted. No conspicuous differences
were found (Table 2).
From the uniformity existing in the seven trees of P. sylvcstris from
Urbana, Illinois, the five trees of P. tacda, and the twenty-six trees of
P. pinaster from the region around College Station, Texas, one would
be tempted to conclude that the trees of a given species growing under
similar conditions have a rather uniform scale number. Contradictory
evidence, however, is afforded by P. Laricio, P. Strobus, and P. montana.
Although the numbers involved leave much to be desired, it is a strik-
ing fact that when grouped according to needle number in a fascicle, the
two-needled pines usually have twelve scales (Fig. 31 A), the three-
needled pines fifteen (Fig. 31 B), and the five-needled pines ten (Fig.
31 C). Sixteen of the thirty-two species counted, including all of those in
which the total number of fascicles counted ran above three hundred, had
nodes which fell at either ten or at fifteen scales per fascicle (Fig. 31 G).
These numbers are equivalent to four and six turns of the phyllotaxic
spiral, respectively, and are twice and three times the basic leaf number
for Pinus as determined by Schneider (79). It is probable that further
counts will show a clear-cut tendency to stabilize the scale number at ten,
fifteen, and possibly at other multiples of five.
It should be pointed out that the pines with deciduous sheaths are uni-
formly low in scale number and that for those with persistent sheaths the
scale number is high. The scale number per fascicle seems to increase
with the length and diameter of the needles, the highest number being
found in P. Torreyana, which has needles unusual as regards both length
and diameter. The second highest numbers were found in the long-leaved
pine, P. palustris.
It is too early to attempt final conclusions in regard to scale numbers
and their significance, and yet there seems to be a definite relation be-
tween scale number and the deciduous habit, and between scale number
and length of leaves, and possibly between scale number and leaf number.
52
ILLINOIS BIOLOGICAL MONOGRAPHS
[176
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EVOLUTION OF P1NUS—D0AK
53
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Fig. 27. — Diagram showing the author's conception of the relation between the
evolution of zonal meristems and the reduction and fusion of parts on the dwarf
shoots and cone scales.
60
ILLINOIS BIOLOGICAL MONOGRAPHS
[184
plained earlier in this paper. Fusions, in general, seem to be the result of
meristematic recession and subsequent zonal growth.
When the leaves of a two-needled pine "fuse," the growing point for
the dwarf shoot may be crowded aside and remain unincorporated
(Fig. 27 t) ; but in the five-needled pines in which all the needles are
fused into a solid column, there can be but one place for the remnant of
the growing point of the dwarf shoot, and that is at the distal end of the
column. If the growing point had not been involved in the common up-
ward growth, it would have remained at the end of the dwarf shoot; in
this event the column would have been hollow instead of solid (Fig. 27 x).
Needles fused in nearly every conceivable manner have been de-
scribed, and proliferated dwarf shoots are also common; yet no case has
been reported in which the proliferated growing point for the dwarf
shoot has been carried up on the fused leaves. According to Masters (57),
such a case was observed for Sciadopitys by Carriere in 1857.
Schneider (79) contends that the fusion of the needles of pines is so
superficial that it is a mistake to compare this condition to the congenital
fusion of Sciadopitys leaves. He believes that the growing point of pines
is never carried up on the leaves, and yet he shows that fusion in pines
can go so far that the double point is entirely eliminated and the double
vascular strand is enclosed in a single endodermal sheath. Both these
conditions go beyond that normally found in Sciadopitys.
Since the seed scale is considered here as a dwarf shoot, we are not
without our example of a transported and proliferated dwarf shoot in this
genus; for Stenzel (86), Willkomm, and others have shown that the
Fig. 28. — Diagram of a series of intergrading involucral bracts, microsporo-
phylls, megasporophylls, seed scales, buds and branches found on various bispo-
rangiate and proliferated cones of the Abictineae.
a, b, c, d, e, f, and g. From Larix europea and P. tonyosho examined by the author,
h and i. From proliferated cones of several genera described in the literature.
185] EVOLUTION OF PINUS—DOAK 61
growing point of the seed scale is sometimes carried up on the tip where
it may make a well-developed dormant bud (Fig. 29 z and z') or even a
leafy'shoot (Parlatore, 68) (Fig. 28 H and I).
The sum of this evidence permits us to link leaf welding with meri-
stematic recession and with zonal growth, and to see that the welding
process can involve vegetative leaves as well as cotyledons, growing
points, and other structures.
4. The One-Leafed Pine (Monophylla)
Since its discovery by J. C. Freemont, Pinus monophylla, now known
as P. cembroides var. monophylla Voss., has been the subject of various
morphological interpretations. In 1874 Bertrand (7) interpreted the leaf
of this pine as a kind of twig, the vascular cylinder of which had opened
and flattened out. In this he seems to have followed Meehan, who had
previously (1872) advanced a twig theory for the interpretation of the
leaves of pines in general as simply the subdivided extension of the dwarf
shoot.
As pointed out by Engelmann (31) it was long considered probable
that the terete leaf of monophylla was in reality a connate pair (Car-
riere, 18). Indeed, such double needles do frequently occur in this as
well as in other pines. This fact led Sir Joseph Hooker (45) to a mis-
interpretation of the true relationship in P. monophylla. He says:
The anomoly of the single leaf is due to the cohesion of the two semiterete
leaves of each sheath and is far from a constant character. In plants at Kew the
two leaves are as often free as united and on making a transverse section it will
be seen that the vascular bundle in the center of the cylinder is in fact double, and
that the two parts are sometimes separated.
This misinterpretation was probably caused by the tendency toward
proliferations and fusions which pines undergo when subjected to ex-
ceptionally favorable conditions. P. monophylla at Kew is under con-
ditions vastly different from those of its Rocky Mountain habitat.
In 1882 Strasburger (87, p. 389) called attention to the facts that the
vascular cylinder of the monophyllous dwarf shoot is open and that the
needle is traversed by a simple rather than a double vascular bundle.
From these facts he correctly concluded that the needle is univalent.
This view had also been expressed by Thomas (90).
In 1913 Schneider (79) advanced convincing anatomical evidence of
a vestigal vascular strand which is present on the rim of the opening
described by Strasburger. The vestige is opposite the functional vascular
bundle and in the position of the vascular strand of the second needle
of two-needled dwarf shoots. Schneider correctly interpreted this as evi-
dence of needle atrophy at this point, but since he worked with mature
dwarf shoots, he was unable to find any external evidence of such atro-
02 ILLINOIS BIOLOGICAL MONOGRAPHS [186
phied needles. Much earlier Masters (56) had seen evidences of such
an abortion. He says:
I investigated the development of the constituent parts of the leaf-bud at vari-
ous stages of growth, and without going into details which are for this purpose
unnecessary, I may say that the development supplied the clue which neither out-
ward morphology nor internal anatomy sufficed to give. In point of fact, in the
earliest stages examined there were always two foliar tubercles, one of which
speedily overpassed the other, so that ultimately all traces of the second leaf were
obliterated
The monophyllous sheath of this pine therefore owes its peculiarity to the
generally arrested development of one of its two original leaves.
This observation, if substantiated with figures and detailed descrip-
tions, would have furnished the complete story and would have prevented
man)- later mistakes in the interpretation of the leaves of this pine. The
view that the leaf of P. monophylla represents an aborted branch was at
first adopted but later rejected by Meehan (60), who, because of further
research stimulated by Newberry (65), changed over to the interpretation
which holds the structure to be a single true leaf.
5. Leaf Reduction in P. monophylla
The presence in monophylla of more needle primordia on the winter
dwarf shoots than ultimately come to maturity (Table 3), at once
centered attention upon this variety as possibly holding the key to the
manner by which the reduction in needle number in pines generally has
been accomplished. Daily observations were made, and a close series of
material was imbedded during the developmental stages.
As growth processes began, the growing point of the dwarf shoot and
one leaf primordi'um (Fig. 25 U) remained inactive while the basal
portion of the remaining needle began the usual meristematic activity
(Fig. 25 A), pressing the differentiating point up into the crest of the
hooded scales ( Fig. 25 B), Soon the meristematic zone seemed to recede
and to spread entirely across the top of the dwarf shoot, thus involving
the inactive primordia in the general upward movement. As these were
lifted into the cylindrical space within the sheath cavity, they became flat-
tened and incorporated in the general mass of undifferentiated cells com-
posing the functional needle. Within a short time both inactive primordia
disappeared completely.
The manner by which this reduction is accomplished is strikingly
similar to that by which the number of primordia is reduced during the
formation of the cotyledons as previously described. Bearing in mind the
suddenness with which the evidences of the manner of reduction disap-
pear, one is not surprised that workers who examined only the mature
leaves and fascicles failed to discover them.
187] EVOLUTION OF PINUS—DOAK 63
On the mature dwarf shoots of other pines, Schneider (79) found
all gradations from complete failure of a part of the needles in a fascicle
to those in which the aborting needles approached the normal size and
development. This frequent occurrence on nearly all pines has been
amply confirmed by my own findings (Fig. 26 and Fig. 1 o). By section-
ing the dwarf shoots on which these vestiges occurred, Schneider showed
that in each case the atrophied trace of the vascular strand was clearly
recognizable. Since he had found a similar trace on the normal dwarf
shoots of monophylla (Fig. 23 G), he was at a loss to explain the absence
of an external vestige from this variety. His conclusion was that the de-
velopment had likely begun but was arrested before the rudiments became
recognizable externally.
6. Leaf Reduction in Other Pines
In order to determine whether the method of reduction of the needle
number observed in monophylla also occurs in other pines, a large num-
ber of young fascicles was examined. Many were found with needle
primordia in excess of the normal number for the species under observa-
tion ; but these did not occur with sufficient frequency to justify the con-
clusion that there would have been a later change toward a lower number,
for mature fascicles with needles in excess of the normal number are
common in nearly all pines. Neither microtome sections nor direct ob-
servations revealed any reduction processes in other species similar to
those taking place in monophylla. The fact that such processes were not
discovered cannot be taken as final proof that they do not occur, but
rather as an indication that other methods of reduction, the evidences of
which are everywhere apparent, must have accounted for most of the re-
duction of the needle number in pines.
The evidences that reductions in needle number have actually been
going on are of such nature and number as to leave little doubt as to
what the general trend has been. Summarized, these evidences are as
follows:
(a) The dwarf shoot, being a specialized branch, must have evolved
from a more generalized branch type. This of necessity could have been
nothing other than the ordinary long shoot with its indefinite number of
leaves. A rudimentary bud with parti)' developed leaf primordia remains
as a convincing evidence of this reduction.
(b) The earliest fossil pines had numerous leaves on the dwarf
shoots, indicating that the trend in leaf number has been downward.
(c) Leaf vestiges and vestigal vascular strands for aborted needles
are common. The two may be associated, or the latter may be present
without the former, as in monophylla.
64 ILLINOIS BIOLOGICAL MONOGRAPHS [188
(d) Varieties or specimens within a species are often found with less
than the usual number of leaves, indicating that reductions are still taking
place.
( e ) Traumic stimuli which would be expected to bring about a re-
turn to primitive conditions cause the needle number to be increased,
marking the higher number as the primitive one.
(f) Dwarf shoots often grow into long shoots with a large number of
needles ; and when this occurs, the branch bears simple leaves and has
other features which suggest this as a primitive branch type.
(g) It is significant that of the related plants with dwarf shoots
Ccdrus, Larix, and Pseiufolarix, which have large and indefinite numbers
of leaves on their dwarf shoots, have scarcely gone beyond the pine-level
in any of their characters, while Sciadopitys and Taxodium with highly
specialized dwarf shoots and fewer foliar organs show a complex of
characters which, on the whole, are more advanced than those of Piuus.
This suggests that dwarf shoot reduction and specialization are associated
with advancement.
7. Increases in Leaf Number
It was hoped that a careful examination of the ontogeny of fascicles
on which supernumerary needles were growing would, in comparison with
that of ordinary fascicles, show significant developmental differences. It
has long been known that the conditions at the time of deposit and exten-
sion may influence the number of needles on the dwarf shoot, for in 1899
Bothwick (9) showed Pin us Laricio, which is ordinarily a two-needled
species, to be capable of producing dwarf shoots with three and four
needles each. For this reason P. Laricio was chosen for determining
whether or not noticeable developmental differences occur. A tree on
which less than two per cent of the fascicles normally had three needles
was selected for observation of the ontogeny of supernumerary needles.
The end and lateral buds distal to the annual growth which had been
extended during the summer of 1930 were completely removed during
the fall of 1930. One or two of the most distal dwarf shoots on each dis-
budded twig, proliferated long shoots during the spring of 1931. These
produced fascicles of which nearly twenty per cent had three needles
each (Fig. 3 y). The ontogeny of these three-needled fascicles, however,
showed nothing which in any way differed from that of pines normally
producing three needles.
The increase in needle number noted above seems to point to a three-
needled ancestor for two-needled pines. Similar evidence is at hand to
support the view that this three-needled ancestor came down from more
remote ancestors which had four and five needles.
189]
EVOLUTION OF PINUS—DOAK
65
Dr. Charles F. Hottes, of the University of Illinois, called attention
to an unusual specimen of a two-needled pine (P. Laricio) which he had
observed over a period of years. This tree was found to be covered with
thousands of young twigs which clothed the trunk to a height of twenty
or more feet. These twigs remain from one to a few years, then die off,
only to be replaced by others of a similar nature. A detailed examination
of some of these twigs revealed astonishing irregularities in needle
number. To illustrate this point a description of a single twig will suffice.
In the spring of 1932 the twig in question appeared as a five-needled
dwarf shoot. This shoot soon proliferated a branch with numerous units,
the foliar components of which were simple with axils mostly sterile.
The axils of five of these simple leaves produced dwarf shoots, and in
each case these had five needles each instead of the customary pair
Table S. — Distribution of Fascicles Having Various
Numbers of Needles From Twigs of One Tree
Number of
Number of
Percentage of
needles
fascicles
total
1
2
100
23
3
281
64
4
2
0.45
5
56
13
6
characteristic of the tree from which the branch was taken. The same
twig continued growth in the spring of 1933. This season it made a
growth four or five inches long, which was covered throughout with
simple leaves. The axils of these leaves bore dwarf shoots, each with
three needles.
A representative sample of similar unusual twigs from the same tree
was gathered, and the fascicles were picked at random until a hundred
normal (two-needled) fascicles had been counted. In order to obtain
this number, 439 fascicles were counted. Among these the needle num-
bers per fascicle were found to be distributed as shown in Table 5.
The most remarkable feature was the paucity of four-needled fascicles
in comparison with five-needled fascicles. The latter, although more re-
mote from the normal, occurred twenty-eight times as frequently as the
former. This suggests five as the basic leaf number and confirms the
view at which Schneider arrived from a consideration of the anatomical
evidence.
66 ILLINOIS BIOLOGICAL MONOGRAPHS [190
8. Factors Determining Leaf Number
As shown by Eichler (29), the cylindrical space within the sheath
determines the cross sectional form of the needle. Needles which grow
alone on dwarf shoots are circular in cross section. Sections of those
grown in pairs, threes, fours, and fives make up halves, thirds, quarters,
and fifths of circles, respectively (Fig. 12 a to e). Since fascicles with
one, four, or six needles are relatively rare, there must be some biological
reason for this numerical discrimination.
Since the sheath plays such an important role in shaping the cross
sectional form of the needle and in making possible its unique zonal
growth, one naturally turns to this organ when seeking the element of
survival which has been responsible for this trend toward certain fixed
■numbers.
It was hoped that the phyllotaxic arrangement of the scales on the
dwarf shoot and the arrangement of needles within the sheath would
throw some light upon the probable reasons for these facts. The leaves
themselves are cyclic, but the phyllotaxy of the other foliar structures
on the dwarf shoot, to which series the leaves undoubtedly belong, follow
the 2/5 scheme. It then becomes clear that, with the progressive shorten-
ing which was necessary in order to eliminate the internodes and produce
the cyclic position, the complete elimination of the internodes from two
turns of the phyllotaxic spiral would bring five needles into a cycle. A
sixth needle, if included, would fall in line with number one and a seventh
in line with number two, and so on, thus setting up interference and
unequal competition within the limited space afforded by the sheath
(Fig. 12 F). Doubtless the phyllotaxic arrangement, coupled with the
crowding of the needles within the sheath, constitutes the major factor
responsible for the preponderance of five-needled species in the genus
Pinus.
Why the reduction should have continued below the number five is
a matter for speculation. The evidence indicates that the decrease below
five must have been a gradual one, the loss of needles being one by one.
If this be true, the immediate forerunner of P. monophylla had two
needles and that of P. Laricio and other two-needled pines had three,
while that of P. palustris had four and so on. Prior to the attainment of
the five-needled condition the reduction must have been at first erratic.
As the internodal shortening proceeded and the cyclic arrangement was
attained, the needles at first must have tended to stabilize at two or more
whorls of five needles each, those of the outer whorl alternating with
those of the inner whorl ( Fig. 12 g). Ample anatomic evidence to sup-
port this view is given by Schneider (79) (Fig. 23 E).
191] EVOLUTION OF PINUS—DOAK 67
The number of needles per fascicle varies considerably with the
species and with conditions. Schneider gives a table showing these varia-
tions in a number of common species.
In seeking to ascertain the reasons for the fact that four-needled and
six-needled types have proved to be less stable than those with three, two,
or five needles, it was observed that in perforating the covering of sheath
scales, the entire fascicle of needles pushes up as a single organ of thrust.
The immediate need is for an efficient perforating organ, for the leaves
must escape from the sheath before their photosynthetic work can begin.
Any arrangement of needles which permits displacement at this critical
stage reduces the combined efficiency and disfavors the survival of the
dwarf shoot whose leaves have such an arrangement. In three-needled
and five-needled fascicles, the planes of separation between the needles
will permit little or no lateral movement, for each needle is wedged
against the two neighboring ones; and the planes of separation are dis-
continuous at the central angle (Fig. 12 c and e). This is not the case
in fascicles with four needles, for here each separating plane extends
from side to side and permits lateral movements of the component needles
(Fig. 12 d). This might possibly displace one or more young needles and
prevent their united action as organs of thrust in perforating the sheath.
A search was made for evidences which would throw light upon this
possibility. P. palustris, which has a complex sheath of many scales and
which in addition occasionally produces fascicles with four needles, was
selected as favorable material for a test. A search was made for those
fascicles from which the needles had failed to escape or from which they
had escaped with difficult}'. These proved to be extremely rare. Since
they usually remain on the tree for only a short time, one must examine
large quantities of late spring or early summer material if fascicles with
crumpled and bound needles (Fig. 19 A and C) are to be found in num-
ber. In order to find nine fascicles of them, approximately 100,000 fasci-
cles were examined. From the same trees from which these were ob-
tained, 5,000 fascicles were selected for determining the needle number
in normal fascicles. Of the 5,000, only nine had four needles each. All
of the others had two and three needles. In other words, approximately
one normally developed fascicle in five hundred had four needles. Among
the fascicles with bound needles, however, three in nine had four needles
each. This is one in three as compared with one in five hundred for the
fascicles with free needles.
Although these results are suggestive, the question of whether or not
the leaf arrangement, which in its turn is a function of the leaf number,
is an important factor in penetration, and consequently in survival, will
await the gathering of more extensive data.
f.S ILLINOIS BIOLOGICAL MONOGRAPHS [192
9. Vascular Supply to the Leaves
As shown by Schneider (79) and confirmed by Aase (1), the vascu-
lar supply to the dwarf shoot arises as two bundles which soon unite
to form a complete vascular ring, from which arise the small bundles to
the various scales. At the top of the ring the bundles to the leaves arise
(Fig. 23 B). It makes little difference whether we are considering the
hard pines in which the bundles to the leaves subsequently divide or the
soft pines in which one "full bundle" without dividing supplies a single
leaf. In either case we may, by combining the vascular supply from a unit
of the long shoot with the vascular supply in a dwarf shoot, get an ar-
rangement such as is shown above.
C. Meristematic Tip, or Bud of the Dwarf Shoot
1. Abnormal (Proliferated) Interfoliar Buds
Distal to the needle attachment and resting at the tip of the dwarf
shoot, the more or less inactive growing point for this modified branch is
usually to be found. From the works of Schacht {77), Dixon (25),
Masters (57), Penzig (69), and others it has long been known that under
certain circumstances these growing points may continue activity and
grow into long shoots (Fig. 5). Sections through the fascicles showing the
normal unproliferated growing points were figured by Strasburger (87).
Dufrenoy (26) points out that the old functional leaves on a pro-
liferated branch serve the proliferated branch in a manner analogous to
that in which the cotyledons serve the young seedling. This is un-
questionably a fact; for the original leaves at the base of such prolifer-
ated branches (Fig. 3 z) usually fall away at the close of the first year,
while on the same tree the leaves on normal non-proliferating dwarf
shoots may remain for four or five years. The increase in diameter of the
dwarf shoot may disturb the vascular supply to the original leaves, or it
may be that the expansion of a bud within causes the sheath to choke the
leaves at their tender bases, resulting in death. The analogy to cotyledons
seems to offer the best explanation for the death of the original leaves,
for in proliferating branches a food gradient is evidently set up from
old leaves to young primordia. This is shown by the arrest of growth in
the leaves of branches proliferating before the maturity of the original
leaves, in which case there is a direct relation between the size of the
proliferated bud and the length of the accompanying leaves (Fig. 18 b).
During the course of the disbudding experiments that were previously
mentioned, it was found that in P. Laricio var. Austriaca one hundred
per cent of the disbudded twigs could be made to proliferate from the
lips of some of their dwarf shoots, usually the most distal ones. Indeed
193] EVOLUTION OF PINUS—DOAK 69
so regularly does proliferation occur in this species that it is possible to
prune back half or more of the annual growth of each twig each season,
thereby producing a small dense tree suited to rock gardens or to other
plantings of limited space. On such a tree all the branches represent
proliferated dwarf shoots. Just such a tree has been maintained for
years at the Horticultural Rock Garden at the University of Illinois.
The disbudded twigs of P. Strobus proliferated twigs from their in-
terfoliar buds to a far less extent than those of P. Laricio. In P. Strobus
not more than one twig in a hundred proliferated at all, and this, during
the first summer following disbudding, took the form of a scale-covered
bud. In P. Laricio branches were often pushed out immediately without
the intervention of dormant buds. Schneider (79) found that P. Strobus
proliferated more readily than did P. sylvestris. Since P. sylvestris is
more like P. Laricio than it is like P. Strobus, this observation may be
taken to be the reverse of what would be expected. Very likely the ability
to proliferate will be found to depend upon the age and vigor of the tree,
but the writer's observations indicate that, other circumstances being
equal, pines with persistent fascicle sheaths proliferate more readily than
those with deciduous sheaths.
2. Normal (Non-Proliferated) Interfoliar Buds
Voluminous and interesting is the literature on proliferated dwarf
shoots, but no extensive researches have been made into the normal
nature and frequence of occurrence of bud rudiments on those normal
dwarf shoots which never proliferate. It is true that Bothwick (10) has
written a short paper on this subject, but he leaves the impression that
these "interfoliar" buds occur on all of the dwarf shoots and that they
are more or less invariable in make-up. Other writers dismiss the subject
with but a word. Jeffrey, in his exhaustive comparison of Prepinus staten-
insis with modern pines (47), leaves the impression that although the
buds are present on modern pines, the}- soon disappear. He says of them:
"The growing point of the short-shoot [of Prepinus] persisted indefi-
nitely and did not disappear at an early stage, as in the living representa-
tives of the genus." Other modern botanists seem to be of the opinion
that such buds do not normally occur. Torrey (92), summarizing the
evolution of the brachyblast, says: "Modern pines rarely have more than
five needles, and have completely lost the terminal bud." In the light of
these views the question of frequency, distribution, and. variation of these
interfoliar buds was undertaken.
A preliminary investigation showed that on some dwarf shoots no
trace of the tip meristems is to be found (Fig. 7 A). When present,
these growing points grade from minute simple domes of meristematic
70
ILLINOIS BIOLOGICAL MONOGRAPHS
[194
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195] EVOLUTION OF P1NUS—D0AK 71
tissue through buds with varying numbers of secondary (foliar) pri-
mordia to well-developed scaly buds (Figs. 7 A). The latter grade off
without a separating line into types already described as proliferated.
There was some indication that the buds grew from year to year without
being actually extended to form branches. For this reason the obser-
vations made to determine the normal interfoliar buds were always made
on fascicles which were in their second year of growth.
In order to make the necessary observations, the fascicle sheaths were
removed and the needles spread apart under a dissection microscope. An
estimate was made of the number of secondary scales present on the
primordium. Eleven classes were made. Those on which there was a
complete absence of primordia were tabulated under zero (Table 6).
Those on which dome-shaped growing points were present but which
were without secondary scales were placed in class one. Those with a
small number of scale primordia were classified according to the esti-
mated number of their scales into classes two to nine. All others, regard-
less of the degree of development, were placed in class ten (Fig. 7 A).
No species was found in which growing points were entirely absent
from all of the dwarf shoots. As would be expected they are less de-
veloped on the pines which have deciduous sheaths ; for in order to be
able to dispense with the sheath, meristematic activity in the entire fasci-
cle, including the intercalary zones of the needles, is cut short. This
arrest undoubtedly affects the adjacent tissues of the interfoliar bud. The
shedding of the sheath exposes the growing point to the sun and drying
air. This exposure has an adverse effect upon the bud's further develop-
ment. These facts, in part, account for the usual low state of the grow-
ing point on the white pines and for the fact that proliferations for these
have been so rarely reported in the literature. They explain at the same
time the low percentage of proliferation obtained from the disbudded
branches of P. Str obits.
In order to determine whether or not the interfoliar buds continue to
grow over a period of years, P. pinaster, because of the fact that its
dwarf shoots are deciduous only after several years, was selected for
study.
In the fall of 1932, large numbers of fascicles were gathered from
each year's growth for the years from 1928 to 1932, inclusive, approxi-
mately equal numbers being taken from each year's growth. These col-
lections were repeated for each of several twigs from each of several
trees. In order to eliminate the human element, fascicles of each age
were placed in separate paper bags ; the bags were then dated with con-
cealed numbers; and after the fascicles had been thoroughly stirred, the
72
ILLINOIS BIOLOGICAL MONOGRAPHS
[196
bags were drawn at random. The condition of 100 primordia from each
bag was determined (Table 7).
The results obtained from these counts showed little evidence of any
growth except for the first and possibly the second years. Buds from
fascicles which were two years old were better developed than those from
three, four, and five-year fascicles. Since bud parts once formed cannot
Table 7. — Annual Growth of Interfoliar Buds of P. pinaster
Year
1
2
3
4
5
6
7
8
9
10
Mode
Average
Age in
years
1928
3
10
3
48
30
6
1
4
4.20
5
1929
2
3
10
66
13
1
2
4
4.11
4
1930
9
13
58
15
1
4
4
3.98
3
1931
4
12
18
28
32
5
1
1
6
4.91
2
1932
10
37
41
9
3
4
3.58
1
be lost and since any differential shedding over the course of years would
tend, by elimination of the most weakly developed fascicles, to raise
rather than lower the average bud condition, we must account for the
high average on 1931 (second year) fascicles by assuming that during
that year conditions for bud formation were more favorable than in the
years immediately preceding.
D. Branch and Leaf Forms in Fossil and
Modern Relatives of Pinus
In selecting a series of fossils with which to illustrate the steps in
the probable evolution of the dwarf shoot, the task is not an easy one,
for some think that pine-like characters have at times been held in com-
mon with other plants which are not abietineous. Jeffrey (47) for ex-
ample says: "The occurrence of linear leaves in fascicles is in itself no
real evidence of Abietineous affinity." While admitting that in some in-
stances it might have been possible to select better representatives from
the endless number of fossil relatives, the following will, nevertheless,
serve our purpose.
i. Pityites
When one reads a summary of fossil Abietineae such as is given by
Seward (81, Chapter 48), he is impressed witli the difficulties of sepa-
rating these plants into the various fossil genera. Because of these diffi-
culties, Seward proposes the group name Pityites for abietineous fossils
which cannot with confidence be referred to a more precise position. The
difficulties created by the interblending of characters is well illustrated
by Pityites Solmsi, the long shoots of which were made up of units with
197] EVOLUTION OF PINUS—DOAK 73
short internodal components. The foliar components fell off and left
persistent bases such as are met with in modern pines. The dwarf shoots
were clothed at the base with scales and bore numerous (10 to 20) long
needles. It is unlikely that any of the scales completely encircled so large
a number of needles. If perforation occurred at all, the encircling fibers
must have been broken early, and any supporting work was due either to
rigid bases or to fibrous entanglements along the adjacent scale margins.
The cones of this plant resembled those of P. Strobus or P. cxcclsa.
Some of the dwarf shoots of Pityites Solmsi were branched as in
Larix (Fig. 24 E, F, and G) and Cedrus, the latter of which it resembled,
though the greater length of needles is more in accordance with that of
recent species of Pinus.
2. Prepimis statenensis
Probably the best-known fossil relative of modern pines was described
by Jeffrey (46), who includes in the summary of his paper the following
important conclusions:
The name Prepinus is proposed for this type in the belief that it is the direct
ancestor of Pinus.
The Abietineae are the oldest living family of the Coniferales.
Pinus is the oldest living representative of the Abietineae.
From the excellent figures and the clear descriptions furnished by
Jeffrey, several significant facts in regard to the morphology of this in-
teresting fossil are manifest.
The dwarf shoot was deciduous, as is evidenced by a single annual
ring associated with resin canals which were occluded by tyloses. The
sheath scales were numerous, and at least the basal ones were shed, leav-
ing marks very similar to those left where the scales of modern pines
break away from a living base. Most of the scales were not deciduous,
and, although there is no evidence of perforation, the crowded and an-
gular leaves show clearly that the sheath exerted sufficient pressure upon
the leaves to shape them into the available space within the sheath cavity.
The reduced and distorted growing point on the dwarf shoot gives a
similar testimony regarding growth pressures. The presence of a scale-
like protective cover around the growing point, marks this as a bud be-
longing originally to a different year's growth from that of the rest of the
dwarf shoot. The elongated angular leaves suggest growth from zonal
meristems, and yet the continuation of resin ducts to the very base, as in
the simple leaves of modern pines, hints that zonal meristems were
probably less specialized than in modern pines.
The leaf trace in Prepinus statenensis remained undivided, resembling
in this respect species of Pinus belonging to the section Strobus, Cembra,
etc.
74 ILLINOIS BIOLOGICAL MONOGRAPHS [198
3. Fossil Pines of Modern Types
Existing in the same forests with Prepinus, there were pines of mod-
ern type, as shown by Jeffrey (46), who figures a transverse section
through the base of a quadrifoliar dwarf shoot of one of these. This
specimen, even to such details as leaf arrangement, leaf shape, and nature
of sheath scale, could pass for a pine of today. The double vascular
bundle in the leaves of this specimen marks it as a hard pine.
Detached leaves from bifoliar dwarf shoots of both hard and soft
pines were also found in the same beds.
Solms-Laubach (84) described leaves of a Pinus-like plant from the
Upper Jurassic or Lower Cretaceous of Bell Island. This plant had
leaves which were oval or circular in outline and had the typical infolding
of the walls of the mesophyll as do modern pines and cedars. The shape
of the leaf made it strikingly like the leaf of monophylla. Solms-Laubach
described the vascular bundle as being single ; this would make the plant
all the more like monophylla. Seward (81), after having examined some
of the material, could find no convincing proof of the singleness of the
bundle. He points out the fact that a second bundle may sometimes be
absent in individual leaves of species normally possessing them. In speak-
ing of this species, Seward says: "It affords an interesting example of an
Abietineous type in all probability of Upper Jurassic age, exhibiting a re-
markable resemblance to certain recent species especially Pinus ■mono-
phylla."
Under the name Pityocladus, Nathorst (64, p. 62) describes branches
similar to those of Pityites Soliusi and of Prepinus. Their occurrence as
detached fossils suggests the possibility of their being deciduous, while
the presence of leaves on some but not on others suggests the possibility
of indifferently deciduous leaves on the dwarf shoot. This is just as one
would expect in a form which was transitional between deciduous leaves
and deciduous shoots.
7. Taxites
An interesting species, which Seward (81) says was first described
by Nathorst as Taxites longif alius, shows an association of flattened and
elongated leaves with scale-covered dwarf shoots. The leaves were from
one to five or more millimeters in breadth and were borne in fascicles of
eight or more. Such plants have been found at numerous widely sepa-
rated points. Leaves of this type may be looked upon as hesitating
between the abandonment of blades and the establishment of zonal
meristems.
199] EVOLUTION OF PINUS—DOAK 75
5. Pityophyllum
Seward (81, p. 380) says:
This name [Pityophyllum] is applied to detached leaves of needle-like form
like those of recent pines, or to long linear leaves broader and flatter than the
needles of Finns. Some of the specimens referred to this genus are very similar
to the leaves of Keteleeria. In a few cases the leaves are still attached to a dwarf
shoot, but usually they occur as detached specimens. The genus is met with in
Rhactic strata but is especially abundant in Jurassic floras and persists through
Cretaceous and Tertiary rocks. The leaves generally described under this generic
term are broader and flatter than such leaves as those of Pityites Solmsi and recent
Pines, and the presence of a fine transverse wrinkling on the lamina is a charac-
teristic feature. Pityophyllum is employed for both the narrower and broader
forms, and includes specimens which in all probability belong to Coniferes of more
than one family. Some are certainly Abietineous but the flatter and broader forms
bear a closer resemblance to the leaves of some species of Podocarpus.
6. Modern Relatives
The morphology of the dwarf shoots of Cedrus, Larix, and Pseudo-
larix is comparatively simple and well understood. The situation in
Taxodium, however, is more complex. Here the portion of the dwarf
shoot which is homologous to the dwarf shoot of pines is partly imbedded
and may be exposed by stripping away the bark (Fig. 20). These dwarf
shoots branch repeatedly from lateral buds which occur at the base of
the current growth (Fig. 21).
The resulting deciduous shoots are homologous to a proliferated dwarf
shoot of pine and not to the ordinary dwarf shoots as interpreted by
Bernard (6). It is as if the dwarf shoot of pines should produce a lateral
bud in the axil of one or both of the lateral scales and then form the
absciss layer just distal to this point, later imbedding this basal remnant
with its bud in the cortex of the primary branch. The following spring
the lateral bud again repeats the process. Such behavior on the part of
Taxodium accounts for the yearly crop of deciduous branches, while
the production of more than one lateral bud leads to branching of the
dwarf shoot and eventually to the tufts of deciduous twigs which are so
characteristic of the old branches of members of this genus.
If Sequoia and related plants have abandoned regular annual branch-
fall in favor of a more or less continuous branch-fall as hinted at by
Bernard (6), it may be that in such plants the homologue of the dwarf
shoot now lies imbedded at the base of the lateral branches. It is con-
ceivable that this has been one of the ways by which the dwarf shoot has
been eliminated from some members of Pinaceae.
These findings are difficult of exact interpretation; but for our
purpose it is sufficient to point out that the forms which were character-
istic of Jurassic and Cretaceous time and which persisted through the
76 ILLINOIS BIOLOGICAL MONOGRAPHS [200
Tertiary had leaves and dwarf shoots, each of a type through which
those of modern pines must, of necessity, have evolved.
The sum of these findings calls to our attention forms with large and
indefinite numbers of scales as well as large and indefinite numbers of
functional leaves on the dwarf shoots, forms with indifferently decidu-
ous leaves, with indifferently bladed leaves, with indifferently developed
zonal meristems, with fascicle sheath scales serving partly developed sup-
porting functions, dwarf shoots with partly suppressed growing points,
tufts of functional leaves which approach the whorled condition, and
flattened fascicled leaves unshaped by sheath pressures. Plants with these
features grew side by side with others which, at this early period, had
evolved characters that we now associate with the most advanced of mod-
ern pines. In short, the fossil record when combined with the better-
known story of the short shoots of modern forms presents a fragmentary
but readable history of the evolution of the dwarf shoots of Pinus.
VI. EVOLUTION OF THE VEGETATIVE DWARF
SHOOT AND ITS FOLIAR ORGANS
A. Literature
In treating the gymnosperms as a whole. Coulter and Chamberlain
(22, p. 406), under the heading of "Evolutionary Tendencies among
Gymnosperms," call attention to the fact that, "A general tendency ex-
presses itself throughout a great group, and has to do with the transition
from ancient to modern forms, rather than with the breaking up of the
group into several phylogenetic lines." Certain of the tendencies to which
they have called attention need be mentioned here. Their conclusion in
regard to "the most obvious tendency to reduce the cotyledons to the
fixed number two" has been mentioned earlier in this paper.
In discussing the tendencies of the leaf, Coulter and Chamberlain say:
It seems clear that the most ancient gymnosperms were large-leaved forms,
from which the small-leaved conifers were derived and yet small-leaved pterido-
phytes may have been more ancient than large-leaved ones. If this be true, the
appearance of small leaves among conifers is the reappearance of an ancient
feature and not its retention.
Coulter and Chamberlain make no mention of internodal shortening
as a general tendency', and yet this change must have accompanied the
transition from macrophylly to the microphylly. Large-bladed leaves on
short crowded nodes such as we find on modern pines is inconceivable.
In order to prevent light interference, bladed leaves on dwarf shoots re-
quire long petioles as in Ginkgo. Indeed, Fankhauser (33) found a close
similarity between the anatomical structure of the petiole of Ginkgo and
201] EVOLUTION OF PINUS—DOAK 77
the leaf of pines. Masters ( 57) thinks that pine needles represent the
petiolar remnant of such a leaf. The macrophyllous leaves of Ginkgo
necessitate a sparse distribution of the dwarf shoots along the twigs
(Fig. 24 B and C). These are often more than 100 times as far apart
as the dwarf shoots of pines. Whether the extreme internodal shortening
in the ancestry of Pinus occurred during or after the acquisition of mi-
crophylly is a debatable point, but it is certain that the short internodes
did not precede the loss of broad blades.
Additional quotations from Coulter and Chamberlain are advisable:
The leaves of gymnosperms may be used to illustrate a structure that exhibits
no general evolutionary tendency, but responds more or less directly to the con-
ditions of living. The most ancient gymnosperms possessed ample, fernlike leaves,
and under appropriate conditions this type of leaf persisted, as in the tropical
cycads of today. The conifers, however, have developed a very different type of
leaf, one that was well under way among the Cordaitales, and which reaches an
extreme expression in small and rigid needles or concrescent scales
It would be interesting to know the conditions in which needles and con-
crescent disks were established: but in the absence of any such knowledge, the
sharply contrasted geographical distribution of Cycadalcs and Coniferales may
suggest that the conditions of change were associated with the evolution of the
land areas and of the climate of temperate regions.
Because of the close relationship between the various components of
a stem unit, it is preferable to treat the evolution of the foliar and the
corresponding internodal component together. In the light of evidences
already cited, an attempt is made to outline the steps as we interpret them.
B. Steps in the Evolution of the Dwarf Shoot
and Functional Leaves
1. Before the advent of branch dimorphism the forerunners of the
dwarf shoots must have been simply the leafy secondary branches
(Fig. 29 a). Since these were in no way different from the long shoots,
the production of simple buds as described for them applied also to the
laterals, thus crowding the first year's growth of the lateral shoots into
simple, scale-covered, axillary buds (Fig. 29 c). Upon extension these
at first must have made ordinary long shoots.
2. Further shortening involved units other than those bearing bud
scales and produced a dwarf shoot with shortened annual growths
(Fig. 29 f). At this level in dwarf shoot evolution, the possibility of
becoming a long shoot likely depended upon position as in Larix and
some other modern forms. The most distal branches were favored, and
they alone had the opportunity to grow into shoots of unlimited growth.
The remaining shoots were miniature replicas of their more favored fel-
lows. In such crowded positions the leaves, in order to prevent light in-
78
ILLINOIS BIOLOGICAL MONOGRAPHS
[202
terference, must have been either linear as in Ccdrus or else lifted on
long petioles as in Ginkgo. A reduction or loss of blades, therefore,
probably paralleled this early development of the dwarf shoot. From this
point the evolution of the dwarf shoot seems to have followed more than
one course. We shall concern ourselves only with that leading to Pinus.
Fig. 29. — Diagrams showing the author's conception of the
chief steps in the evolution of the dwarf shoot.
(See explanation on opposite page.)
203]
EVOLUTION OF PINUS—DOAK
;<>
3. Further shortening crowded the leaves, even after extension of
their short internodes, back within the cup (forerunner of the sheath)
formed by the old bud scales. This protected the leaf bases from me-
chanical and insect injury, and from drying, thus permitting the basal
cells to remain tender and meristematic. The acquisition of zonal meri-
stems gave the power of continued growth, thus permitting an adjust-
ment of needle size to the season. This overcame the handicap imposed
by the acquisition of compound buds, for in these the number of units
for a given season is unchangeably fixed during the season prior to their
functioning, so that the leaf number cannot be adjusted to later
changes in climatic conditions. With the advent of basal meristems it
became possible to limit or to increase the photosynthetic area without
changing the leaf number.
Crowding of the leaves within the cup or sheath limited tip growth
of the dwarf shoot to a single annual growth; consequently these shoots
soon fell behind and were shaded off. Branch- fall came to have survival
value, and the deciduous habit became fixed. With the establishment of
branch- fall, it became poor economy to store much food in the dwarf
Explanation
a. Hypothetical early ancestor with
monomorphic branches and
monomorphic leaves.
b. Section of the same showing sub-
tending leaf in black and the po-
sition of the primary stem in a
broken arc.
c. Simple axillary bud.
d. Lateral branch showing well-marked
annual growth.
e. Transverse section of same showing
bud scales surrounding the stem.
f. Twig similar to d, but with leaves
crowded and blades lost.
g. Transverse section of same showing
leaf bases within the circle of
bud scales.
h. Twig similar to /, but further short-
ened and deciduous (white line
represents absciss layer).
i. Transverse section of same showing
sheath scales specialized for sup-
port.
j. Twig similar to /;, but further short-
ened.
k. Transverse section of the same
showing crowded angular leaves
and reduced interfoliar bud.
1. Dwarf shoot of Pinus.
m. Same in transverse section.
n. Dwarf shoot of Pinus with fused
needles.
of Fig. 29
o. Same in transverse section.
p. Dwarf shoot of Pinus cembroides
var. monophylla.
q. Same in transverse section.
r. Simple sterile leaf as in Larix.
s. Transverse section of same showing
sterile axil.
t. Concrescent scale leaf as in Cupres-
sus.
u. Transverse section of same.
v. Dwarf shoot of Sciadopitys show-
ing loss of sheath and fusion of
needles.
w. Transverse section of the same.
x and x'. Exterior and sectional view
of a reduced axillary seed scale
on a proliferated shoot from the
cone of Abies (after Willkomm).
The tissues of the reduced scale
render the base of the leaf con-
crescent.
y. Proliferated shoot from cone of
Abies (after Willkomm).
z. Portion of a twig similar to r ex-
cept the seed scales are well de-
veloped and each bears a bud at
the tip (after Willkomm).
z'. Single unit from z but more highly
magnified (after Willkomm).
80 ILLINOIS BIOLOGICAL MONOGRAPHS [204
shoots or to use materials in the construction of woody parts soon to be
lost. Further elongation of the leaves at the expense of the shoot was the
natural consequence. The tendencies toward leaf extension and shoot
shortening were thus accentuated.
It is extremely unlikely that these early dwarf shoots acquired at once
any of the highly specialized features such as perforated scales or
whorled leaves. For this reason we would postulate for this stage in the
evolution of the dwarf shoot, a short, weakly, deciduous branch whose
basal bud scales supported several close spirals of leaves of the typical
conifer type and whose tip formed a poorly developed scale-covered bud
for the following year's growth. To put the case in other terms, this
stage in the evolution of the dwarf shoot was approaching the Prcpinus
level (Fig. 29 j and k).
4. We have only to assume the continued shortening of internodes
in order to arrive at the condition found in Prcpinus statcncnsis. Here
the deciduous habit was well established and the interfoliar bud reduced
and crowded out of shape. The sheath scales were highly specialized
and evidently exerted sufficient pressure upon the enclosed leaves to shape
these to the cylindrical space within the sheath.
5. The compound winter bud on the long shoot had several far-reach-
ing effects upon the dwarf shoots which in their early stages came to be
enclosed within it. This enclosure relieved the scales of the dwarf shoot
of the work of meristematic protection, this function having now been
taken over by the primary (subtending) leaves. The scales on the dwarf
shoot were thus left free to exercise their newly acquired function of
leaf support. Hooding, fraying, perforation, zonal growth, and the
various means for shedding the sheath now came as adaptations to the
supporting function. The young buds for the dwarf shoots were crowded
together within the compound bud, where competition for space was keen.
Growth pressures were exerted upon the meristematic secondary shoots ;
their proximal scales (lateral and central scales) were displaced and
flattened, and certain leaf arrangements were favored.
6. The delay which was responsible for the compound winter bud
necessitated the almost simultaneous extension of the main twig, of all
the dwarf shoots, and of the leaves. This in turn necessitated the forma-
tion of all these structures out of stored foods. The limited amount of
growth possible from this source tended to shorten still further the inter-
nodes on the primary axis, to bring the dwarf shoots into interference
with each other, and to put an additional premium upon a long-continued
growth of the needles.
7. Further specialization of the sheath scales, especially the advent
of perforation, increased the binding efficiency of these organs. The
205] EVOLUTION OF PINUS—DOAK 81
leaves were crowded and their corresponding internodes shortened to
extinction, and the needles were brought into the cyclic position. The
cyclic arrangement necessitated a limitation of leaf number to harmonize
with the phyllotaxy, and dwarf shoots with five needles or with some
small multiple of five needles were favored. The acquisition of these
features together with a continuation of the reduction of the interfoliar
bud marked the advent of the true pines (Fig. 29 1 and m).
On occasional dwarf shoots in nearly all pines and in the so-called
monophyllous varieties in several species, meristematic recession involves
all the leaves in a common upward growth, producing a single structure
from the welding or cohesion of several leaves (Fig. 29 n and o). This
carries the evolution one step beyond that attained by the group as a
whole. With reference to its tip meristem and functional leaves, at least
one related form, Sciadopitys, became stabilized at this level. In this
genus an additional reducing step has been taken, for Sciadopitys has
eliminated the scales of the fascicle sheath.
8. In some respects one variety (mono phylla) of P. cembroides car-
ries the reductions beyond the point attained in Sciadopitys. Here the re-
cession involves the incorporation of extra leaves into a single functional
one with but a vascular vestige of the other contributing member. Thus
is produced the most highly specialized condition found in the vegeta-
tive dwarf shoots of any modern pine (Fig. 25 A; Fig. 29 p and q). The
sheath, although still present in monophylla, is here reduced in number
of parts and in complexity of scales.
9. There is some evidence in support of the view that shoot reduction
has at some time in the past gone far beyond the point now found in
either Sciadopitys or in P. cembroides var. monophylla. The reduction
of dwarf shoots to the point of extinction is not inconceivable. If this has
been the course of evolution, we should not be surprised to find fossil
plants with pine-like characters but with extremely reduced phylloclads in
the axils of simple leaves, or simply a proliferation of axillary tissue to
produce an adhesion of leaf and stem. Following the production of such
a reduced structure, the next step would be the complete loss of the
axillary outgrowth. Thus by the complete elimination of dwarf shoots,
pine-like ancestors may have given rise to other genera such as are now
described as having monomorphic branches (Fig. 29 r, s, t, and u).
C. Evolution of the Leaf Meristems
The important steps in the phylogeny of leaf meristems which we find
in pines appear to have been as follows:
1. Apical as in ferns (Fig. 27 a, b, and c). Buchholz (IS) has shown
that this condition is still retained in the early embryos of pines.
82
ILLINOIS BIOLOGICAL MONOGRAPHS
[206
2. Grouped or general as in most simple leaves.
3. Basal as in the needle leaves of pines (Fig. 27 g and i).
4. Sub-basal as in P. ccmbroidcs var. monophylla, in fused pine
needles, and in the seed scales (Fig. 27 j to x).
t
T
t /^
1
SO Bud Scalee--Gi
oup B. /
b
1 / ,-
I-
¥ -~ < ? f>mil«.
te Conee.
1
T
1
/ r, -.
al Buds,
\
1
Fertile Series.
1 56 Dwarf Shoots.
c
■a
o
1 1
1 I
i
1 /
SO Stamlnate '-i.ee.
o
\ 1
•If
Axis.
a
a
T /
/20 St
1 /
t
erile Braote of The Male
i
Sterile Series
I
a
\ /
30 Bud Soales--Group i
1
I
f
U 1 .7
August
Sep.
Fig. 30. — Annual curve of deposit of units on the long axis.
VII. THE OVULATE DWARF SHOOT, OR SEED SCALE
A. VOLTZIA AND THE PRIMITIVE TYPE OF SEED SCALE
Numerous fossils have been described which throw some light upon
the structure of the primitive abietineous cone scale, but our discussion
will be confined to the single excellently preserved specimen of Voltzia
Liebeana which Walton (100) figured (Fig. 32, parts 4 and 5) and de-
scribed in 1929.
Voltzia was obviously a conifer, the seed scale of which was woody,
flattened, multisporophyllate, and transitional between the greatly reduced
seed scales of modern conifers and the simple strobili (Fig. 32, parts 1
and 2) out of which the scales of both Voltzia and modern conifers
must have evolved.
207] EVOLUTION OF PINUS—DOAK 83
On Walton's specimen the leaf-like cover scale was unmistakably
present. The constituent sporophylls of the branch-like seed scale were
five in number. The first pair were opposite each other, and in both shape
and position resembled the lateral scales of the vegetative dwarf shoot.
Although somewhat crescent-shaped in cross section (Fig. 32 cs), these
lateral sporophylls had their seed-bearing surfaces turned away from the
cover scale and toward the axis of the compound strobilus of which they
were originally a part.
The individual sporophylls each bore a single seed, which is the exact
number found on the sporophylls* of members of both the Abietineac and
Araucarineae.
The central sporophyll of Voltzia occupied a position exactly cor-
responding to that of the central scale on the vegetative dwarf shoot of
Pinus. It was more flattened than the lateral sporophylls and was not
folded, a fact which shows that the direction of pressure was along the
axial plane. The apex of the central sporophyll was directed upward.
The long axis, while lying in the axial plane, paralleled that of the main
axis of the compound strobilus. If the central sporophyll had an opposing
mate on the cover-scale-side of the axis, this was so much reduced that
it remained hidden by the cover scale.
The two sporophylls that remained were flattened, sterile, and laterally
placed. They occupied the concavities formed by the folding of the lateral
sporophylls.
During fossilization of Walton's specimen, the growing point of the
scale was hidden in such a way that the presence of a terminal-bud-
vestige was left uncertain. Our experience with dwarf shoots in general
and with cone scales in particular leads us to believe that a terminal bud
of some kind must have been present. Reason demands the presence
of such a growing point, at least during the early stages, for we cannot
conceive of the presence of five well-developed foliar organs without
assuming an axis out of which their early primordia were developed. We
have a choice, then, of assuming the presence of an axis on the mature
scale or its absence due to incorporation during the development of the
scale.
With this brief description we shall leave Voltzia for the moment and
return to it in connection with the treatment of the evolution of the cone
scale of conifers in general.
B. Developmental Morphology of the Normal Seed Scale
The early developmental stages of the seed scale are amply treated by
Strasburger (87, Plate V) who makes a comparative study of them as
*The morphological sporophyll is here referred to. It is not to be confused with the seed
scales.
84 ILLINOIS BIOLOGICAL MONOGRAPHS [208
seen in many conifers. He, from a study of the normal anatomy and de-
velopment, arrives at the brachyblast interpretation of the seed scale.
In the present work the similarities between the earl)' stages in the de-
velopment of the dwarf shoot and the corresponding stages in the de-
velopment of the cone scales were found to be striking (Fig. 22). The
bract or cover scale for the latter, as pointed out by Strasburger (83), is
without question homologous to the subtending scale of the former. Both
give rise to axillary outgrowths (Fig. 22 A and F) which, because they
grow from the axils of homologous organs, are themselves homologous.
In both cases these axillary outgrowths in their turn give rise to a pair of
simultaneously appearing lateral primordia (Fig. 22 B and G) which, by
the same rule, are homologous. In other words, the megasporophyll of
the seed scale is homologous to the lateral scales of the fascicle sheath.
The primordia for the lateral megasporophylls are more robust and
appear earlier in the ontogeny of the axillary outgrowth than do the
lateral scales of the fascicle sheath (Fig. 22 B and G). In Pinus, simul-
taneous meristematic activity in all three primordia of the cone scale lifts
the triple-pointed structure upward until the center member finally ceases
meristematic activity and matures all its tissue, thus becoming the apophy-
sis (Fig. 22 H and I).
The lateral sporophyll primordia differentiate vascular strands and
become the two flattened lateral extensions of the seed scale, and each
bears a single ovule. The three fused structures collectively make up the
seed scale (Fig. 28 g and f).
Since in its early stages the median member resembles the growing
point of the dwarf shoot, Strasburger interpreted it as the axis of the
dwarf shoot. The unquestioned presence of this structure demands that,
regardless of whether it be interpreted as a true axis or as a third sporo-
phyll or as some other structure, some disposition be made of it ; for,
while differentiating its own vascular supply, it becomes welded in as an
integral part of the connate seed scale. The question yet to be settled,
however, is whether the primordium and the vascular strand subsequently
differentiated represent vestiges of a foliar or an axial structure. Dis-
cussion of this point will be deferred until all contributing evidences
have been presented.
C. Abnormalities of Bisporangiate Cones
Ordinarily the cones of members of the Abietineae are monosporangi-
ate. but numerous descriptions of exceptions may be found in the litera-
ture. Stenzel (86) found on one occasion in Picea excelsa Link:
.... androgynous cones, in which the male organs usually occupied the base and
the female the upper part ; more rarely were the male scattered amongst the
209] EVOLUTION OF PINUS—DOAK 85
female; and still more rarely did the male form a middle zone with female above
and below. Some of the bracts bore pollen-sacs.
Miss Holmes (44) describes, in one of the latest articles on this subject,
a bisporangiate cone of Tsuga canadensis which was without transitional
scales. She gives a partial summary of the literature dealing with the
subject and points out the fact that similar cones have been found in
most abietineous genera.
In the spring of 1932, the present writer discovered seven bisporangi-
ate cones of Larix enropea, most of which showed scales of various tran-
sitional and deformed types. These were carefully removed in order from
the base of the cone upward, and a serial record was made of the char-
acters of each scale.
Although bisporangiate cones in this species are not new (Bartlett, 4),
it was hoped that the series of transitional scales would reveal some evi-
dences of the morphology of the abietineous seed scale. When the scale
records for the individual cones were arranged in parallel, certain very
suggestive trends were apparent. Before this material could be assembled
for publication, hundreds of bisporangiate cones of Pinus tonyosho
(Fig. 14) and two cones of P. Laricio were discovered.
After numerous specimens of the pine material had been examined
and serial records of the transitional scales on each had been made, most
of the scales were observed to fall naturally into the classes which had
already been made for Larix. The same general trends were observed
here as were recorded for that genus.
The following description will be clearer if the reader will refer
frequently to the series of accompanying diagrams (Fig. 28). In most
cases scales of the following types were found on each cone examined
and in approximately the order given:
1. At the base there were the usual involucral bracts which on normal
pollen-producing cones precede the microsporophylls. In Larix these are
green and in appearance closely approach the functional leaves (Fig. 24
G; Fig. 28 a).
2. Next in series followed the normal microsporophylls with their
characteristic paired and abaxial pollen sacs (Fig. 28 b and b').
3. As the region of transition was approached, there was a strong
tendency toward reduction and final disappearance of one of the pollen
sacs while the remaining one tended to assume a median position (Fig.
28 c and c').
4. At about this level the pollen sacs began to produce rudimentary
micropylar apparatus (Fig. 28 d) and otherwise to assume the appear-
ance of ovules, while various aborted structures began to appear in the
axils of the microsporophylls.
86 ILLINOIS BIOLOGICAL MONOGRAPHS [210
Above this level the behavior became far more erratic. Every con-
ceivable type and combination of abnormal cover scale and seed scale
were found. Some types appeared but once, and many others could not be
fitted into any series. Most of the types, however, fitted into the regular
series and were repeated on cone after cone.
Continuing our description of the regularly recurring types we have:
5. Nearly normal microsporophylls bearing micropylar apparatus on
each sporangium and with rudimentary seed scales in the axils of the
sporophylls, as shown in Fig. 28 (d), except with two microsporangia
instead of one.
6. Cover scales with bladed portions similar to those appearing on the
microsporophylls and at the same time bearing single median ovules on
their abaxial surfaces and normal seed scales in their axils.
7. Leaf-like cover scales with two-lobed fleshy sterile seed scales in
their axils.
8. Leaf-like cover scales with axillary structures consisting of fleshy
seed scales divided to their bases (Fig. 28 g).
9. Forms similar to those described above (paragraph 8) but with the
median member obviously welded into one of the members of the divided
scale.
10. Forms similar to those described above (paragraph 8) but with
blade-like expansions on some of the constituent megasporophylls.
11. Normal-appearing seed scales, the ovuloid structures of which
were full of pollen.
12. Cover scales which in color and texture were identical with the
seed scales and in some cases bore normal-appearing ovules on their
abaxial surface. In one case the cover scale was so much like the two
members which constituted the seed scale that had it not been for the
point of the apophysis, it would have been impossible to determine which
pair in the trio belonged to the seed scale. In other words, the cover
scale was in the latter case transformed into a normal megasporophyll.
13. Finally the transitional zone and irregular structures gave way to
normal cover scales which bore normal seed scales in their axils (Fig.
28 f). From this point to its apex, the cone was then, as a rule, normally
ovulate.
The general impression gained from this array of material is that
during the period of deposit of cone units, some physiological upset
reversed the trend of development. Sporophylls which ordinarily would
have produced two microsporangia began by stages to approach the
megasporophylls in texture, in product, and in number of sporangia, and
during the course of transition produced every conceivable transitional
form. If, as suggested by Fujii (36), the sporophylls are at first indif-
ferent as to type and their course is later determined by nutritional con-
211] EVOLUTION OF PINUS—DOAK 87
ditions, the present observations are just as would be expected of a series
of sporophylls formed during a period of nutritional change.
From the standpoint of the interpretation of the seed scale, it is sig-
nificant that the number of sporangia per sporophyll becomes reduced to
one, and that this assumes a median position at the same time that the
microsporangium is acquiring micropylar apparatus and other characters
ordinarily associated with ovules. The inference seems clear: the micro-
sporophyll in Pinus has a pair of sporangia, while the megasporophyll
has but a single sporangium. This is further attested by the presence of
but a single ovule on the abaxial side of those cover scales which assume
the color and texture of the seed scale. This is especially noteworthy
since these cover scales were in direct series with normal microspo-
rophylls and they in turn with leaf-like involucral bracts.
It is also significant that, at a stage during which the megasporophylls
that ordinarily fuse to form the seed scale are remaining free from each
other, many of them develop expanded blade-like tips, indicative of their
foliar nature.
Of further significance is the fact that various constituents, which
ordinarily fuse to make the seed scale, can be found as single, double, or
triple rudimentary elevations, and that only two of these bear ovules.
If only one ovule is present, the point of the apophysis can usually be
seen fused against the side of the unilateral scale as would be expected
if one of the sporophylls had failed while the other had in the usual way
become fused with the median member. If two ovules are present, they
are on a scale that approaches the normal, i.e., double-pointed and
flattened, or else they are on the divided halves of such a scale — indicat-
ing that the sporophylls normally fuse, but at times fail to do so.
Occasionally these divided scales have between them at their bases a
third rudiment, which, with reference to the cover scale, occupies a posi-
tion approaching the axillary. Since in no case this central structure
bore either an ovule or a bud, the material afforded no direct evidence as
to whether the central structure represented the shoot axis as proposed
by Strasburger or a third and sterilized sporophyll as proposed by
Celakovsky. The position of this structure could not be used to argue
alone for its cauline nature ; for, as will be shown later, this argues
equally as strongly for its sporophyll nature.
From the sum of the evidence certain facts seem indisputable. It is
clear that in Pinus there are three parts which normally fuse to make
the seed scale. Of these, the two lateral members normally bear one
ovule each.* The third or median member normally makes the apophysis.
*The fact that one ovule per sporophyll seems to be normal for Pinus does not preclude
the possibility that some members of the Pinaceae may have sporophylls which are multiovulate;
otherwise we would have to assume an incredibly larye number of sporophylls in the scales of
such forms as Sequoia and Cupressus.
88 ILLINOIS BIOLOGICAL MONOGRAPHS [212
It is sterile, axillary in position, and therefore represents either an axis
or a sterilized central sporophyll. The cover scale is foliar and is homol-
ogous to the microsporophyll ; it may or may not be involved in the
fusion of parts. The ovulate cone, as this evidence testifies, is a com-
pound structure ; and the seed scale is, therefore, a modified short shoot,
or brachyblast.
D. Abnormalities of Monosporangiate and Proliferated Cones
It is remarkable how other teratological forms of an entirely different
nature from those summarized above force us to similar conclusions with
regard to the nature of the seed scale. I refer to what is commonly called
proliferated cone scales. The persuasive power of these structures is well
illustrated by the fact that Willkomm (102), despite his previous adher-
ence to the placentation theory of Schleiden and of Sachs, from a study
of proliferated cones of Abies, came to agree with the brachyblast in-
terpretation. Botanists in general have tended to adopt this view, and in
numerous instances it has been such proliferated cones which provided
convincing evidence of the correctness of the theory. The literature list
of such proliferated cones is a long one. It includes the following:
Parlatore — Pinus Lemoniana (68).
Oersted — Picca ? Larix sp., Pinus Montana (67).
Sperk — Cunninghamia, Cupressus lusitanica (85).
Stenzel — Picca excelsa, P. alba, Tsuga Brunoniana (86).
Willkomm — Picca excelsa (102).
Velenovsky — Larix (97).
Caspary — Spruce (19).
Celakovsky — Spjruce sp. ? (21).
Noll— Larix sp. ? (66).
Engelmann — Sequoia.
Rraun — Taxodium, Crypiomaria, Glyptostrobus (11).
In spite of this array of evidence, not all modern botanists agree upon
the brachyblast interpretation of the seed scale. Jeffrey (46), for ex-
ample, apparently considers the evidence inadequate. He says (p. 337):
The view sometimes advanced that the ovuliferous scale in the Abietineae
consists of a fused pair of foliar structures has apparently no evidence in its favor.
It is as clearly a single leaf as is the microsporophyll.
The axillary structures which Willkomm (102) found on proliferated
cones of Abies may be taken as representative (Fig. 19 z and z') of the
scales on proliferated cones in general. This material and that found on
my own bisporangiate cones of P. tonyosho are supplementary, for while
213] EVOLUTION OF PINUS—DOAK 89
the former shows transitional stages between foliage leaves and cover
scales, between cover scales and microsporophylls, and between micro-
sporophylls and megasporophylls, the latter shows transitional stages be-
tween the sporophylls and true leaves and between the apophysis and the
central constituent of the scale (Fig. 28 e and h).
In order to weld every link in this chain of metamorphosis from
leaves through bracts, microsporophylls, and megasporophylls finally to
the welded scale, it is only necessary to review the marvelous array of
structures described by the workers cited above. A complete review of
all the tell-tale individuals in the perfectly blending series is out of the
question. We must be content with a partial description of a few repre-
sentative specimens. The descriptions are taken largely from Worsdell's
(104) excellent summary of this subject. He says:
In 1876 Stenzel described a cone in which in the axil of the bract a leafy bud
arose, whose first two leaves were harder and browner and more erect than those
of the ordinary vegetative shoot, and resembled more the seminiferous scale; they
were directed somewhat towards the axis ; the following pair of leaves were median,
anterior and posterior [Fig. 32, pt. 20]. No ovules were to be seen. The pair of
larger first leaves were often fused with the small leaves of the bud. He [Stenzel]
concludes that 'the seminiferous scale of the Spruces consists of the first two leaves
of an otherwise undeveloped branch arising in the axil of the bract, these leaves
being fused by their posterior margins, and thus having their dorsal side directed
towards the axis of the cone, and bearing each on this side an ovule.'
He [Stenzel] also possessed at this time a proliferated cone of Picea alba.
The buds in the axils of the bracts bore, besides the two seminiferous scales fused
by their posterior and gaping at their anterior margins, a posterior and an anterior
scale, and one or two inner scales. In some cases the seminiferous scale was so
completely fused with the anterior bud-scale as to form a single flat scale as seen
from the front, but in reality its posterior margins were represented by two low
ridges, visible from the inside, which did not, as in other cases, extend as far as
the posterior bud-scale. As regards the characteristic projection or 'Dorn' on the
seminiferous scale of P'mus, which Strasburger thinks is an axis, it may represent
either the place of fusion of the posterior margins of the seminiferous scale, or the
posterior bud-scale.
It is significant that this description of a proliferated scale could, with
a few minor changes, pass for a description of the scale of Voltzia, for
the "anterior bud-scale" here referred to is clearly equivalent, not only to
the central sporophyll of Voltzia, but to the whole series of anterior
structures shown as S' in the sketches comprising Fig. 32. The presence
of "one or two inner scales" makes the resemblance to Voltzia almost
complete.
The same kind of sports as those in Picca occur in Tsuga Brunoniana. In the
latter plant, the posterior bud-scale is often as well developed as the anterior one,
so that the parts of the bud all come to be united laterally into a woody structure.
The axis of the bud is often more elongated into a leafy shoot.
Here again we have parts similar to those in Voltzia but with a pos-
90 ILLINOIS BIOLOGICAL MONOGRAPHS [214
terior mate for the central scale and with a well-developed terminal bud
for the brachyblast.
Caspary and Oersted found cones of more than one genus which in
many respects were like the bisporangiate cones of P. tonyosho, described
earlier in this paper. Many of their cones, however, had additional de-
velopments in the form of buds on some of the central members. They
thus furnished convincing evidence of the branch nature of such scales.
In the proliferated Sciadopitys cones described by Masters, the seed
scales were replaced by the regular double needles w-hich are generally
admitted to be brachyblasts. Masters concludes: "Whatever be the nature
of the so-called leaf of Sciadopitys [Fig. 32, part 15], it must be essen-
tially the same as that of the seed scale of Abietincac."
Velenovsky in 1888 described a cone of Larix on which one axillary
bud "bore ovules on the lower surface of all its leaves" (Fig. 32, parts 1
and 2).
Certainly such proliferated scales, by the very frequence of their
occurrence, argue strongly for the brachyblast interpretation of the ab-
ietineous cone. Of this, Celakovsky seems to have been full}' aware.
In this connection, Worsdell quotes him as follows:
In the Abietineae the seminiferous scale is "a symphyllodial structure, con-
sisting of three fused appendages (two in Picea) of an axis, of which the two
lateral are fertile carpels (reduced to sporangia) fused together to form the 'crista'
of the seminiferous scale, while the third median leaf — the median knob of the
first rudiment — remains sterile, and either aborts or, fused with the two other
fertile carpels, forms the keel and mucro (in Finns)."
This view has not been given the attention that it deserves; for, if
the "anterior bud-leaf" mentioned by Velenovsky is a constituent of the
normal seed scale, it follows that the middle member of the three primor-
dia on the young cone scale (Fig. 22 G) is not the primordium for the
axis but rather the primordium for the central sporophyll. The growing
point of the axis either has been completely suppressed or is incorporated
into the central sporophyll.
There are some who, in spite of the frequent recurrence of these
ativistic forms and the regularity of arrangement of their parts, still hold
that such structures are meaningless abnormalities. This view is hardly
tenable, for structures w-hich occur regularly on plants of many genera
and yet maintain a more or less constant form can hardly be called mon-
strosities, especially when early fossil forms like Voltzia Licgeana bring
direct evidence to support the view that the observed forms represent
true reversions. Careful comparison with 1'oltzia causes the doubt re-
garding the meaning of separated multifoliate parts of the seed scale to
disappear, and the presence of buds and branches at the tips of the cone
scales to become fraught with evolutionary meaning.
215] EVOLUTION OF PINUS—DOAK 91
E. Vascular Supply and the Scale of Araucaria
In summarizing her description of the vascular supply to the cone
units of Pinus, Aase says, "In all cases four bundles result, the lower
supplying the bract [cover scale], the remaining three the scale [seed
scale]." In similar terms we might summarize Aase's findings with ref-
erence to Araucaria by saying that, in all cases four bundles result, the
lower three supplying the bract, the remaining one the scale (Fig. 23 O
to V). If the four bundles are homologous throughout, it simply means
that in Araucaria the two lateral sporophylls instead of the central one
have been sterilized, reduced, and welded into the scale. In keeping with
the greatly exaggerated size of the cover scale in Araucaria, the lateral
scales, although fused with a common structure consisting of four parts,
apparently derive their vascular supply from the sides of the bundle lead-
ing to the cover scale (Fig. 23 U, V, and W).
With the idea that the functional sporophyll in Araucaria represents
the central sporophyll, Celakovsky would agree, but not to the welding in
of the lateral sporophylls. Worsdell says of Celakovsky's opinion in this
matter: "In the Araucarieae where the seminiferous scale, bearing a
single ovule, is obviously not a compound but a single organ, the scale-
consists solely of the leaf or its sporangial representative, the first leaf
pair of the axillary bud being entirely absent."
Eames (28) in 1913, in a paper on Agathis, summarized the seed scale
situation in general and concludes that, in origin, it is compound in all
Coniferales; with reference to the group under special investigation he
says, "Even within themselves the Araucarineae show a complete series
from a form with strobilar units of a distinctly double nature to one most
simple through reduction."
Sinnott (83) is of the opinion that both podocarps and araucarians
have evolved from ancient abietinean stock and that the epimatium of
podocarps, the ligule of araucarians, and the scale of Abietineae are all
homologous structures and vestiges of axillary shoots. He thinks the
simple scale of the podocarps has arisen either from the fusion of the
two constituents of the. abietinean scale or by the abortion of one of them.
This derivation of the araucarian scale and of its one functional spo-
rophyll component is not the same as that suggested by Celakovsky ; for
to derive the single functional sporophyll directly from a J'oltzia-like
ancestor by sterilization of the lateral sporophylls is quite a different
thing from deriving first the abietinean type of scale and then, out of this,
by further reductions, deriving a simple scale with a single functional
sporophyll. Sinnott's interpretation would make the functional sporophyll
of Araucaria the homologue of one of the lateral sporophylls, while that
of Celakovsky would make it the homologue of the central scale.
92 ILLINOIS BIOLOGICAL MONOGRAPHS [216
VIII. EVOLUTION OF THE OVULATE DWARF SHOOT,
OR SEED SCALE
A. Leading Ixterpretational Theories
Although a brief restatement of the principal views relative to the
morphological interpretation of the cone scale will probably help us to
see the significance of the contributions made in the present paper, it
would not be profitable for us to discuss in detail the numerous interpre-
tations which have been placed upon this structure, for they are amply
treated by Radais (71), Worsdell (105), Coulter and Chamberlain (22),
and others.
The leading theories have been:
1. A calyx, Linnaeus (52).
2. An open carpel, Robert Brown (12).
3. A placental or ligular outgrowth from the cover scale, Schleiden
{7S), Sachs (75), and Willkomm (early works, 101).
4. Two fused leaves of an axillary branch or two leaves fused against
the side of the axillary branch, Alex. Braun (11), Von Mohl (98, 99),
Strasburger (87 and 88), Willkomm (late works, 102), Velenovsky (97),
Celakovsky (20), Noll (66), Thiselton (89), Saxton (76), and a number
of others.
5. The first and only leaf of an aborted axis. Van Tiegheim (96) or
a simple axillary megasporophyll, Jeffrey (47).
6. A chalazal outgrowth from the ovules, Bessey (8).
In the formulation of this array of theories, nearly every known
branch of botanical science has contributed arguments for or against the
various views. The chaotic condition of the whole problem serves to
emphasize the fact that the final solution cannot be expected to come
from isolated bits of information but rather from the accumulation of
evidences from many fields, and by a new evaluation of the old evidences
from all fields.
By a careful examination of the list of interpretations given above, it
will be seen that following the discovery of gymnospermy (1827) only a
small group of workers have interpreted the cover scale as being equiv-
alent to the sporophyll. These may be grouped together, for they would
make the seed scale a simple sporophyll and the entire cone a simple
strobilus. All the other interpretations would make the cover scale a
subtending bract and the entire cone a compound strobilus. In all the
theories in the latter group, the seed scale is interpreted as a secondary
axis of limited growth and, therefore, a dwarf shoot (brachyblast).
The differences between the various interpretations in this group arise
in the effort to decide just how short this ovuliferous short shoot really is.
117]
EVOLUTION OF PINUS—DOAK
93
Is it so short that the axis fails entirely and only a single sporophyll
appears on the spot where the shoot disappeared, or is it just short
enough for the true axis to put in its appearance and then produce in
turn one, two, or more foliar organs? After all, these are but questions
pertaining to the extent of shortening, and the various interpretations,
excepting those of Sachs and Bessey, are seen to be not very different
one from the other.
Had the various workers proposing these theories observed the com-
parative ontogeny of seed scale and vegetative dwarf shoot, had they seen
an abundance of integrading scales and sporophylls, had they been ac-
quainted with Voltzia Liebeana as described by Walton, and had they
taken into account the vascular anatomy as described by Aase, Eames,
and Sinnott, there is little doubt that all would have been united upon the
brachyblast interpretation. None, then, would have felt constrained to
Scale Number and
_ dumber.
NeedloN'
®m
Two -need lei
Fines.
10 11 12 13
Scale "umber and Condition
of Sheath.
Q.
D. Deciduous Sheathed
Species.
V,
/.
U2
t:i
,
m
F. Scale dumber
All Species
Based on Modes.
7
n
9 10 11 13 1314 15 16 17 18 19^0 21 22
/
B. Three-needled /
Fines. j
EX
1213 14 15
yj C. Five-needled
V, Pines.
/
IA
8 9 10 U 12 13 14 15 16 17 18 19 20 21 22
£. iers intent -sheathed
Speoies.
n
10 1112 13 14 15 16 17 19 19 ZO 2122
G. Total Counts
All Species.
H. TJeedle
^unberB on
rascloles of
30 Q Ab normal Tree.
i
1011121314 15 16 171819 20 2122 Per. Fas. i 23 4 5
Fig. 31. — Graphs showing fascicle scale numbers in relation to
needle number and persistent and deciduous sheaths.
A. Scale numbers on the fascicles of E. Same for pines with persistent
two-needled pines. sheaths.
B. Same for three-needled pines. F. Scale number on all species based
C. Same for five-needled pines. on nodes.
D. Scale number on the fascicles of G. Scale number on all species based
pines with deciduous sheaths. on total counts.
94
ILLINOIS BIOLOGICAL MONOGRAPHS
[218
defend a set number of sporophylls as having been retained by all con-
ifers, but instead would have been free to admit of variations in number
of constituent sporophylls in the seed scale. In Araucaria this number is
made up of one functional sporophyll with vascular remains of two
others; in Abietineae it is made up of two functional and a single ves-
tigial sporophyll with frequent reversions to more ; in Voltcia the number
is three functional and two vestigial. The whole range of forms marks
out tendencies which point unmistakably to lost forms with a large and
indefinite number.
Fig. 32. — The author's conception of the chief steps in the evolution of the
cone scale. The lettering throughout is uniform, a representing the cone axis and
a' the axis of the simple strobilus or cone scale, c.s. the bract or cover scale, and
s, s' , s", etc., the various sporophylls. (See explanation on opposite page.)
219] EVOLUTION OF PINUS—DOAK 95
B. Summary of Steps in Cone Scale Evolution
In order to see how the seed scale may have been phylogenetically
produced, one has but to assume a repetition here of processes known to
have taken place in other parts of such plants as the pine.
1. The same foliar reduction processes which have for geological ages
been operating on the vegetative dwarf shoot of Pimts and related forms
have operated also upon the ovulate dwarf shoot, reducing its foliar
organs (sporophylls) to a single functional pair.
2. The same internodal shortening (to disappearance), which brought
cotyledons and functional leaves into cyclic positions, and the lateral
scales of the vegetative dwarf shoot into positions opposite each other,
has, in an analogous manner, brought the first foliar pair on the ovulifer-
ous dwarf shoot into basal positions directly opposite each other.
3. The same pressure between subtending leaf and main axis which
flattened the base of the dwarf shoot and displaced the three most prox-
imal of its attached foliar organs, has here flattened and displaced the
sporophylls.
4. The same meristematic recession which involved in a common
intercalary growth the adjacent cotyledonary primordia on the embryo,
the adjacent leaf primordia on fascicles of fused needles, the adjacent
leaf and growing point primordia on the dwarf shoots of monophylla, has
here again produced a compound ("fused") organ.
5. The same process of incorporation by maturation, which eliminated
extra cotyledonary growing points from the embryo, and extra leaves as
Explanation of Fig. .i2
1 and 2. Front and back views of 12. Transverse section of the same.
the hypothetical early simple 13. Mature seed scale of Finns Lam-
strobilus. bertiana.
3. Transverse section of the same. 14. Transverse section of the same.
4 and S. Front and back views of Volt- 15. Diagram of section through base
sia Licbcana G. (redrawn and of the double leaf of Sciadopitys
relabelled from Walton). showing the absence of central
6. Probable transverse section of same and lateral scales.
with the shed seed and the axis 10. Diagrammatic section through base
supplied. of dwarf shoot of Finns.
7, 8, and 9. Back, side, and sectional 17. Diagram of Sperk's abnormal scale
views of typical cone scales from of Cunninghamia as described
the proliferated Abies cones de- by Worsdell.
scribed by Willkomm (redrawn 18. Diagram of Caspary's abnormal
and relabelled from Willkomm). abietinean scale (relabelled from
10. Same but with axis reduced, fused Worsdell).
parts separated, and with seed 19. Diagram of araucarian scale,
supplied. 20. Diagram of a scale from Stenzel's
11. Scale of Pinus tonyosho which by abnormal cone of Picea (from
the failure of the usual fusions his description),
show's the separated constitu-
ents of the scale.
"<> ILLINOIS BIOLOGICAL MONOGRAPHS [220
well as a superfluous growing point from the dwarf shoots of P. mono-
phylla, has here eliminated extra sporophylls and the growing point of
the ovulate dwarf shoot.
From forms with numerous widely separated sporophylls displayed in
simple strobili, the evolution of the cone scale gave rise to forms with
successively shorter and shorter axes and with fewer and fewer spor-
ophylls.
] T oltzia with its fertile lateral pair of sporophylls, its fertile central
sporophyll, and its sterile vestiges of more distal sporophylls, represents
hut a step in the shortening and reduction processes.
From J'oltcia-like forms, evolution followed two lines. In one case,
reduction and fusion of parts and the sterilization of the lateral spo-
rophylls gave rise to a single-seeded scale containing but one functional
sporophyll which, however, became an integral part of an apparently
simple seed scale as in Araucaria. This superficially simple seed scale
has been derived from the welding of the bract, two sterilized lateral spo-
rophylls, and a functional central sporophyll.
In the line leading to the Abictineae the retention, modification, and
welding of the primary pair or lateral sporophylls together with the
sterilization of, and in some cases the loss of, the central sporophyll, gave
rise to the scale as we now find it in this group.
C. Advantages of the Brachyblast Interpretation
This view has the following advantages:
1. It is in keeping with the views held by the most careful workers
in the field.
2. It brings into harmony many of the apparently conflicting views of
previous workers by" showing these views correct as far as they go; for
in the absence of complete information regarding the details of develop-
ment, partial interpretations should be regarded as incomplete and not
necessarily as incorrect.
3. By this view the two most characteristic structures found in Pinus,
i.e., the dwarf shoot and the seed scale, become homologous and explain-
able by the same evolutionary tendencies.
4. It accounts for all the primordia which appear in the axil of the
cover scale.
5. It homologizes the microsporophylls and megasporphylls as well as
the axes upon which these are borne.
6. It is in agreement with the finding of buds, dwarf shoots, and leafy
shoots in the axils of the cover scales and makes intelligible the wide-
spread occurrence and regular form of these structures.
7. It lends meaning to the divided, partly-fused, and triple-pointed
scales on bisporangiate and proliferated cones.
221] EVOLUTION OF PINUS—DOAK 97
8. It derives the abietineous and the araucarian cone scales from a
common type and points to known structures to explain the vascular
anatomy of both.
9. It makes intelligible the finding of single ovules on the lower sur-
faces of foliar constituents of axillary buds and explains why, when the
bud is suppressed, the two lower sporophylls "orientated themselves" with
reference to the axis (Velenovsky, 97).
10. It lends eloquence to the otherwise discordant Lar'xx cone de-
scribed first by Velenovsky, one scale of which bore "besides the two
fleshy placental lobes, five other fleshy ovule-bearing scales," and makes
this scale and the short statement about it speak clearly for the branch
origin of the scale.
11. It is in keeping with the finding of multisporophylled seed scales
in early fossil gymnosperms and points, for the origin of both araucarian
and abietinean cones, to a type the existence of which is well established.
12. It fixes well-marked tendencies which will account for the condi-
tions found in the cones of Sequoia, Cupressus, and Taxodium without
involving additional processes ; for a continuation of internodal shorten-
ing coupled with meristematic recession w-ould certainly soon involve the
primordium of the subtending scale (cover scale) in the common upward
movement and in the fusion. It is conceivable that incorporation by
maturation might also apply to this primordium, thus accounting not only
for the fusion of seed scale and cover scale but also for the disappearance
of the latter from those forms in which little or no trace of it can be
found.
IX. THE PHYLOGENY OF THE PINACEAE
No doubt the members of the family Pinaceae have had a common
ancestor, and since the Abictineae, the oldest tribe in this family, show a
strong leaning toward dwarf shoots, it is likely that the common ancestor
had dwarf shoots. This is evidenced by the fact that four of the nine
genera in the Abictineae (Pinus, Cedrus, Larix, and Pseudolarix) have
this feature. In Cedrus, Larix, and Pseudolarix the dwarf shoots are of
a rather generalized type, and on the whole the associated characters arc-
primitive.
Three of the eight genera in the tribe Taxodineae (Sciadopitys,
Taxodium, and Glyptostrobus) have dwarf shoots, and in every case
these unquestionably represent extremes of dwarf shoot specialization.
These are on the whole associated with more advanced characters than
are the dwarf-shoot-bearing members of the Abietineae. The more ad-
vanced tribe of Cupressineae has ten or eleven genera with no vegetative
dwarf shoots among them. The evidence suggests that the common
98 ILLINOIS BIOLOGICAL MONOGRAPHS [222
ancestor of all Pinaceae had spur shoots of a non-specialized type and
that such branches have been lost from most of the genera and have
become highly specialized in the majority of those which have retained
them.
We find ourselves projecting the established evolutionary trends of
shortening, recession, elimination, and rneristematic fusions against the
background of the Pinaceae and inquiring as to what characters would
show in a line of plants in which the tendencies to reduce the dwarf shoot
had brought this structure to the vanishing point towards which we have
seen it so steadily carried. One has but to strip the dwarf shoots from a
pine in order to see what type of plant would be produced by the loss of
these organs. Our hypothetical plant can then be constructed by applying
to this "disbranched" pine the tendencies already well established.
The leaves of such a plant would certainly be microphyllous, even
scale-like (Fig. 29 r and s), as occur almost universally in the family
Pinaceae. The axils would be for the most part sterile, and those which
remained fertile would produce long shoots with probably an occasional
reversion to the dwarf shoot condition as found in Abies, Pseudotsuga,
etc. Conservative portions of our hypothetical plant, especially when
wounded or otherwise unduly stimulated, would be expected to show
some trace of the ancient dwarf shoot character, as do the seed scales of
all Abietineaeous cones and the cone axes of proliferated individuals
from many genera. The trend toward internodal shortening would no
longer be hampered by the necessity of keeping the dwarf shoots prop-
erly distributed. This shortening, if continued, would lead to the com-
plete elimination of internodes, thus producing opposite and cyclic leaves
just as we find in the Cupressineae. With the axillary shoot eliminated
and the primary leaf alone remaining, further fusions by intercalary
growth could do nothing except to produce adnation of the primary foliar
organ with the internode of the primary axis. Indeed the presence of a
trace of the old dwarf shoot meristem in the axil would be expected to
favor such a course (Fig. 29 x, x', and u). This would produce a con-
crescent leaf as in certain members of the Cupressineae (Fig. 29 t and u).
It is clear that, instead of describing a hypothetical plant, our descrip-
tion fits well the features associated with higher members of the family
Pinaceae. So numerous and varied are the points of agreement that on
a basis of dwarf shoot evidence alone, we can safely assume that evolu-
tion of the Pinaceae has been from a common ancestor with generalized
dwarf shoots as in Cedrus, through forms with more and more highly
specialized dwarf shoots as in Prepinus, Pinus, Sciadopitys, Taxodium,
etc., to forms from which the dwarf shoots have been eliminated as in
Abies, Pseudotsuga, etc., and finally to forms with opposite and concres-
cent leaves as in Cnprcssus.
223] EVOLUTION OF PINUS—DOAK 99
For phylogenetic purposes it is unsafe to consider dwarf shoots, or
cone scales, or any other single structure alone. One should rather con-
sider all the known characters of the organism with which one is work-
ing. Sinnott's work on Podocarpus (83) well illustrates this fact. He
effectively compares the characters of the Abietineae and Podocarpincae
to support the derivation of the fruiting structures of the latter from the
cone scale of the former and to argue for connecting these two groups
on the phylogenetic tree. The mass of evidence would support such a
connection, and yet we prefer to leave open the question of where to
connect the line leading to the Podocarpincae until we know more def-
initely whether the single functional sporophyll of Podocarpus represents
the central sporophyll or one of the lateral sporophylls.
In nearly all forms the evolution of the vegetative dwarf shoot and
that of the ovulate short shoot have gone hand in hand. Forms like
Larix and Ccdrits have primitive short shoots associated with relatively
primitive seed scales ; Sciadopitys and Taxodium with highly specialized
short shoots have advanced cone scales ; and forms like Cupressus,
Junipcrns, and Araucaria, from which the dwarf shoots have been lost,
have the most highly specialized cone scales found among the members
of the Pinaceae.
From this general agreement between the evolution of the dwarf
shoot and the seed scale, only Picca, Tsuga, Abies, and Pseudotsuga are
out of line, for these forms, although devoid of short shoots, still possess
seed scales which are at the Pinus level. Since the bulk of characters for
these plants is primitive, it is necessary to assume that while advanced
in one character they have remained primitive in many others.
Our conclusions with reference to phylogeny are: that the Arauca-
rincae and the Abietineae separated early from a common ancestor; that
there is some doubt as to which of these lines gave rise to the Pod-
ocarpincae and Taxodineae ; that among the Pinaceae, Cedrus and Larix
are low, Preplans and Pinus intermediate, Sciadopitys and Taxodium
high, and Cupressus the highest in position.
X. SUMMARY
1. A study is made of the axial and foliar systems of about thirty-five
species of pines and of a few related plants.
2. The constituent units of the tree are described in their order of
appearance.
3. The ontogeny of the cotyledons supports the view that polycoty-
ledony is a primitive character and that fusions, incorporations, and
reductions mark advances.
100 ILLINOIS BIOLOGICAL MONOGRAPHS [224
4. The natural and abnormal occurrence of simple leaves is treated,
and their artificial production through wounding is demonstrated.
5. In the ontogeny of the bud scales it is shown that the interlocking
fringed margins are the product of several factors including a hooding
of the primordium, an angular arrangement of the marginal tissues, and
the expansion of underlying parts which in some cases actually perforate
the overlapping scales.
6. A technique is described whereby the number of bud scales and of
sterile bracts can be approximately determined prior to extension of the
buds which contain them. This technique is utilized in following the
time of origin of units within the bud.
7. The bud scales are divided into groups "A" and "B" based upon
the time of origin and upon the amount of extension of their respective
internodes.
8. The expansion of the winter bud into the annual growth is de-
scribed.
9. Normal and abnormal sequence of deposit is followed, and evi-
dence is given supporting the view that the so-called lateral cone is an
ecologic rather than a fixed character.
10. The staminate cone axis is considered homologous to the dwarf
shoot, and the ovulate cone axis homologous to the long shoot.
11. Seed cones with proliferations and abnormal sequence of units are
described, and the nature of their abnormalities is used to support the
theory that they represent modified long shoots.
12. The ovulate cone is considered a compound strobilus, and the cone
scale a simple strobilus.
13. The origin of concrescent leaves is associated with the disappear-
ance of dwarf shoot's from the primary axes.
14. The ontogeny of the dwarf shoot and of its foliar organs is given
in detail and the following facts established in regard to them:
a. The first two scales are laterally placed, opposite each other ; and
the first three are distinct from the other scales.
b. The encircling sheath is produced by the perforation of the scales
and the exaggerated overlapping of the scale margins.
c. The dwarf shoot spends the winter rest in full possession of all of
its foliar structures including the needles.
d. Both scales and needles grow from basal (zonal) meristems.
15. In the pines which have deciduous fascicle sheaths, the shedding
of the scales involves the loosening of the cohering portions and the de-
tachment of the scales from the shoot. These steps are accomplished
differently in the different pines.
16. The pines with persistent sheaths crumple these until they cover
225] EVOLUTION OF PINUS—DOAK 101
only one-fourth to one-third as much of the leaves as when fully ex-
tended.
17. The scale numbers per fascicle from representative samples of
thirty-two species and several varieties have been counted and the results
tabulated. The numbers are too variable to be of much taxonomic value,
but certain tendencies are manifest, notably the tendency to stabilize the
scale number at either two or three times the basic leaf number (2x5
or 3 X 5).
18. The early ontogeny of the leaf is given, and its manner of per-
forating the overlying sheath is shown.
19. The orientation of the needles within the sheath is not a constant
character but in some species approximates constancy.
20. The needles are found to fuse in various ways.
21. Fusions are linked with internodal shortening and meristematic
recession.
22. The ontogeny of the dwarf shoot of Pinus cembroides var. mon-
ophylla is essentially like that of other pines except that only one of the
two original leaf primordia comes to maturity, the other needle, together
with the growing point of the dwarf shoot, being usually incorporated
into the functional leaf but without differentiation of vascular tissues.
Similar incorporations were not found in other pines.
23. Dwarf shoots on disbudded branches showed an increase in the
number of leaves, thus marking the reduced number as a derived char-
acter.
24. The basic leaf number of needles is five. This is equivalent to
two turns of the phyllotaxic spiral.
25. A theory of interference is advanced to account for the tendency
toward stabilization at five needles.
26. Inefficiency in perforating the sheath scales has probably dis-
favored stabilizations of pines with four needles.
27. A growing point or interfoliar bud is present between the needles
of most of the dwarf shoots in all the species included in the study.
28. The degree of development of these buds depends both upon the
species and upon the conditions of growth. They develop least in tin-
pines which have deciduous sheaths.
29. Disbudding of the long shoots induces proliferation of some of
the interfoliar buds on the more distal dwarf shoots.
30. Numerous abnormal (bisporangiate) cones of Pinus and Larix
are described in which the ovuliferous scales show non-fused and transi-
tional conditions which, in general, support the brachyblast theory.
31. The brachyblast theory of the cone scale is strengthened by the
fact that the early ontogeny of the dwarf shoot proves to be almost
identical with that of the cone scale anil by the fact that the three most
102 ILLINOIS BIOLOGICAL MONOGRAPHS [226
proximal and most regularly placed scales on the dwarf shoot all have
similarly placed counterparts on the cone scale.
52. The two sporophylls on the seed scale correspond to the lateral
scales on the dwarf shoot.
33. Some of the fossil relatives of Pinus are reviewed.
34. The dwarf shoot of Pinus is found to be homologous with the
persistent basal (imbedded) portion of the shoots of Taxodium, the
deciduous portion of which corresponds to proliferated pine fascicles. It
is pointed out that a discontinuation of the habit of seasonal branch-fall
may have given rise to forms like Sequoia, in which the true homologue
of the dwarf shoot of Pinus may have disappeared simply by being im-
bedded and by having its habit of shedding discontinued.
35. Most of the unique vegetative characters in Pinus can be directly
or indirectly attributed to influences incident to the formation of the
compound bud. This structure relieved the sheath scales from the work
of meristematic protection and permitted specialization along other lines.
It necessitated the almost simultaneous development of many structures
from stored food and exerted shaping pressures upon the enclosed imma-
ture dwarf shoots.
36. Tentative steps in the evolution of the leaf meristems of pines are
presented as follows: (a) apical, (b) grouped, (c) basal, and (d) sub-
basal (in certain special cases).
37. The early common ancestor of the Pinaceac probably was macro-
phyllous and had monomorphic branches.
38. The formation of dimorphic branches accompanied the transition
to microphylly, and the development of the two was probably inter-
dependent.
40. The disappearance of the dwarf shoots and a continuation of the
tendencies toward internodal shortening are postulated as explanations
for the appearance of abietineous forms with opposite, whorled, and
concrescent leaves.
227] EVOLUTION OF PINUS—DOAK 103
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