THE FRUIT OF OPUNTIA FULGIDA
A STUDY OF
PERENNATION AND PROLIFERATION IN
THE FRUITS OF CERTAIN CACTACE/E
BY
DUNCAN S. JOHNSON
QK4-95
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PUBUSHED BY THE CaRNEGIE INSTITUTION OF WASHINGTON
WASHINGTON. 1918
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ibrary
THE FRUIT OF OPUNTIA FULGIDA
A STUDY OF
PERENNATION AND PROLIFERATION IN
THE FRUITS OF CERTAIN CACTACE/E
BY
DUNCAN S: JOHNSON
PUBUSHED BY THE CaRNEGIE InSTITLT
WASHINGTON. V.
THIS BOOK IS DUE ON THE DATE
INDICATED BELOW AND IS SUB-
JECT TO AN OVERDUE FINE AS
POSTED AT THE CIRCULATION
EXCEPTION: D
earlier if this item
MAY/|,j 20ID
e due will be
is RECALLED
150M/01 -92— 920179
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■'/-■(■
CAENEGIE INSTITUTION OF WASHINGTON
Publication Xo. 2G9
BALTIMORE, MD., U. 8. A,
CONTENTS.
PAGE
Comparison of the fruit of Opuntia fulgida with those of other angiosperms. . 5
Vegetative structure of Opuntia fulgida 8
Reproductive organs of Opuntia fulgida 9
Origin and structure of the flovi^er 9
Development of the wall of the ovary with its tubercles 9
Structure and fate of the leaves of the ovarian wall 10
Areoles or axillary buds of the ovarian wall 11
Number, size and distribution of the areoles 12
Origin of the growing point of the areole and sequence of initia-
tion of its organs 12
The trichomes of the areole 13
The nectaries of the areole, their distribution and morphology. ... 14
Spines or thorns of the areole, their distribution, structure, and
fate 15
Bristles or spicules of the areole, their number, structure, and
fate 16
The perianth, stamens, style, and stigmas, their development and
abscission 17
Morphology of the ovary 20
The fruit: Its structure, persistence, and fate, normal and abnormal. ... 25
The fruit at the time of abscission of the perianth 25
The mature fruit 27
The perennating fruit: Its structure and secondary growth 29
The seed : Its structure, persistence, and germination 32
Proliferation of flower and fruit 35
Proliferation from attached flower buds 35
Proliferation of persistent attached fruits 37
Proliferation of fallen fruits 38
Causes and significance of perennation and of the diverse types of
proliferation 41
Proliferation of flower or fruit in allied species 47
Proliferation of joints and fruits in relation to the sterility of fruits 51
Summary and conclusions 53
Literature cited ..._• 56
Explanation of plates % 57
FRONTISPIECE
A mature plant of Opuntia fukjuhi on reservntion of Desert Laboratory at Tucson, showing
a frequent type of forked trunk, due to injury of main axis, also the branching habit
and clusters of fruit. The nesting bird is the cactus wren, Heleodytes hrunneicapillm
couesi (Sharpe).
THE FRUIT OF OPUNTIA FULGIDA.
A STUDY OF PERENNATION AND PROLIFERATION
IN THE FRUITS OF CERTAIN CACTACE/E.'
By DUNCAN S. JOHNSON.
This paper embodies a discussion of the occurrence and significance of a
number of striking peculiarities in the development and fate of the per-
sistent, self-propagating fruits of certain opuntias. The discussion will be
concerned primarily with the perennation and vegetative propagation of the
ovary of Opuntia fulgida. This cactus has been chosen for special consid-
eration because of its most remarkable power of budding off secondary
flowers from the primary ones and also of fonning new flowers and vegeta-
tive shoots from the long-persistent fruits.
This investigation has been aided by grants from the Department of
Botanical Research of the Carnegie Institution of Washington. Acknowl-
edgment is here made to Director D. T. MacDougal for making available
to the writer the facilities of the Desert Laboratory at Tucson, Arizona, and
of the Coastal Laboratory at Carmel, California. The principal parts of
the work have been done at these two laboratories. Other portions ol it
and much of the writing of this paper have been done at the Harps-vN-ell
Laboratory, at South Harpswell, Maine, and at Johns Hopkins University.
Acknowledgment is also made, for aid in securing material, information, or
photographs for this study, to Drs. Forrest Shreve and Hermann Spoehr, of
tlie Department of Botanical Research of the Carnegie Institution, to Dr.
David Griffiths, of the Bureau of Plant Industry, United States Department
of Agi-iculture, to Dr. J. 'N. Rose, of the Smithsonian Institution, and to Dr.
N. L. Britton, of the INTew York Botanical Garden.
COMPARISON OF THE FRUIT OF OPUNTIA FULGIDA
WITH THOSE OF OTHER ANGIOSPERMS.
One of the almost universal characteristics of the fruit in augiosperms is
the comparative brevity of its development. The whole duration of this,
from the inception of the flower to the ripening of the fniit and it^ fiual
separation from the pareut plant, or its opening for the discharge of its
seeds, is usually less than a year, often very much less.
The phases of this developmental cycle of the fruit which can usually be
distinguished are: First, a j^eriod of initiation and maturing of the parts
of the flower, which opens for pollination at about the time an egg has been
' Botanical contribution from The Johns Hoplvins University, No. 56.
5
6 THE FRUIT OF OPUNTIA FULGIDA.
formed in the embryo sac; secondly, there follows soon after pollination,
which is usually succeeded by fertilization, a period of active vegetative
growth of the ovary and often of other parts which are to enter into the
make-up of the fruit. While the fruit is thus growing to its mature size
the seeds are also taking on their characteristic form and size. Thirdly,
accompanying or immediately succeeding the final maturing of the seeds, a
process of ripening occurs in the fruit. During this ripening process the
outer tissues, the niesocarp and epicarp of the fruit, may soften to form a
juicy pulp. In this case the starches, distasteful glueosides, acids, tannins,
alkaloids, etc., which are often present in the cells of this pulp in the green
fruit, are transformed into the sugars, mild acids, and other tasteful flavors,
and often also into brightly colored glueosides that make the fruits attractive
to animals. While these changes are taking place in the outer layers of the
fruit the inner layer, the endocarp, may harden to form the firm stone that
protects the seed when it is eaten by animals. In other types of fruits, as in
pods and capsules, the ripening process involves a drying out and hardening
of all the tissues of the fruit.
Ripening of the fruit is usually followed, often very promptly, by ita
separation from the plant or by its dehiscence and the discharge of its seeds.
Either of these two fates of the fruit involves the more or less immediate
death of its tissues, aside from the seeds. In a few fruits, such as that of
palms like the coconut or the pomes of the Eosace^e, certain tissues of the
fruit may remain alive for some weeks or months after separation from the
parent plant. The growth occurring in these cases is, however, compara-
tively slight and it does not give rise to new buds or new plants.
In the cases of certain opuntias, chiefly cylindropuntias, the fruits differ
from the usual type characterized above in several very remarkable particu-
lars. In the first place the fruits do not ripen with the maturing of the
seeds, but continue to grow actively without undergoing the usual softening
and change of color and of chemical composition so characteristic of the
ripening process of most fleshy fruits. Secondly, the fruits of 0. fulgida
are not shed from the plant when the seeds are ripe, but usually remain
firmly attached and growing, year after year. Thirdly, these attached
fruits (or even the unopened flowers), may, in situ, give rise from their
axillary buds to from one to ten secondary flowers and fruits. A few weeks
later these secondary flowers may give rise in the same way to tertiary ones
and these in turn to quaternary ones. Thus, three or four generations of
flowers and fruits may be produced, all in a single blooming season of three
or four months. Tourthly, if the fruits become separated from the plant
and fall on moist soil^ the same axillary buds which in the attached fruits
would form nothing but flowers will, in the fallen fruits, give rise to
vegetative shoots and roots and to these only. Finally, the embryos of the
ripe seeds, inclosed in the persistent, attached fruits, retain their power of
germination for many years.
THE FRUIT OF OPUNTIA FULGIDA. 7
Certain of the peculiarities above noted in the frnits and seeds of Opuntia
are, it is true, found in a few other plants, though in none of which the
writer has found record is there such an aggregate of unusual features of
development, and certain of these features are unlaiown outside the genus
Opuntia.
The persistent attaclnnent and continued gTo^^i;h of the fruit just noted is,
as far as I can learn, recorded for but one other family of angiosperms, the
Myrtacea). In the genera Callidemon and Melaleuca, for example, the
fniits may persist for 10 or 15 years. In the former, according to Ewart
(1907), the fruit opens and discharges the living seeds only when it has been
killed by the cutting off of its water-supply. This latter may happen in
consequence of severe drought, of the breaking off of the branch bearing it,
or from the death of the branch or whole tree from fire or other cause.
There are, however, three important differences between the behavior of
the fruits of this Australian " bottle-brush " tree and those of such opuntias
as the " choUa " (0. fulgida). In the first place, the persistent fruit of
Callistemon does not possess axillary buds and therefore does not, like
Opuntia, give rise to secondary and tertiary flowers and fruits from these.
Secondly, the fruits of the bottle-brush tree, though they may open and dis-
charge their seeds with the first cutting off of the water-supply, do not them-
selves fall from the tree until some time after they are dead ; hence, they can
play no part in the vegetative propagation of the species. Thirdly, the
seeds of Callistemon are ultimately shed from the fruit to play the most
important role in the dissemination of the plant, while the seeds of the fleshy
fruits of Opuntia fulgida are, as we have seen, never discharged and appar-
ently rarely germinate under natural conditions.
From this comparison of the opuntias with the only other family of plants
having fruits with similar peculiarities, it is clear that these Cactacese have
become much more abnormal as regards the behavior of propagative struc-
tures than any other family of angiosperms. Moreover, the readiness with
which a growing-point destined to give rise to a flower may be induced to
form a vegetative shoot (by the mere separation of the fruit bearing it from
the parent plant) suggests the possibility of discovering here some of the
causes detennining the production from the same meristematic mass, in one
case of a reproductive organ or in another of a vegetative shoot.
With this much of suggestion of the structures and phenomena we are to
deal with, we shall now examine more closely into the development and fate
of the flower, fruit, and seed of certain opuntias. We shall be concerned
primarily with those of Opuntia fulgida, in which these structures have been
studied most carefully in Tucson, Carmel, and Baltimore. Incidentally we
shall also note the structure and capacity for propagation of the vegetative
joints of certain species, in order that we may compare with them the
structures and phenomena observed in sprouting fruits.
8 THE FRUIT OF OPUNTIA FULGIDA.
VEGETATIVE STRUCTURE OF OPUNTIA FULGIDA.
Opuntia fulgida is a tree-like, Sonoran species of Cylindropmvtia, which
commonlj grows to 2 or 3 meters in height and forms a rather irregular flat-
topped crown. The older or main branches are horizontal, or ascendant at
their bases, but bent do^vn at their tips by the weight of the thick terminal
branchlets and often of the large clusters of fruits (fig. 1). The spiny
trunk is dark brown in color, woody in texture, and may reach 20 or 25 cm.
in diameter. The main branches, which are woody like the trunk, may
become 8 or 10 cm. in diameter. The ultimate branches at the end of the
first season's growth are often 3 to 5 cm. in diameter and 15 to 25 cm.
long. These younger branches taper abruptly at the ends and the lateral
surfaces are provided with prominent and somewhat elongated mammillae
or tubercles (figs. 4, 5, 9a). Each tubercle, at this time, bears at its upper
end from 7 to 12 sheathed spines and the growing-point of a lateral bud
(figs. 4, 95). The number of spines in each areole steadily increases with
age, and hence a branch 10 years old may bear 50 spines in each areole.
The leaf to which the areole is axillary is a small and veiy transient structure
which (on falling) leaves only a minute scar, like that to be seen on the
fruit (figs. 5, 47). The vascular system of the stem is net-like in arrange-
ment, being of the same general type as that described and figured by
Ganong (1894, fig. 7). During the first year the bulk of the new joint is
made up of the mucilaginous pulp of the pith and cortex. The latter has
a well-developed photosynthetic and aerating system of the type to be
described in dealing with the fruit, and large numbers of slime-cells {cf.
Wetterwald, 1889, fig. 19). Chloroplasts are abundant throughout the
whole thickness of the cortex of the stem and may even occur within the
zone of woody bundles, as happens in the projecting tubercles. With the
increase in thickness of the branch the woody cylinder seems to gTOW in
diameter more rapidly than the fleshy cortex. The latter finally becomes
stretched and smoothed out and the cortex of the mature stem is compara-
tively thin and dry (fig. 2, at base).
On some plants of this species, as has been noted by Toumey (1895), cer-
tain of the new joints may remain relatively short and have less prominent
tubercles and fewer spines, becoming thus rather fruit-like in form (fig. 7a).
These joints are readily detached and on moist soil may give rise to new
plants by proliferation, just as the ordinary vegetative branches of this and
many other opuntias may do.
THE FRUIT OF OPUNTIA FULGIDA. 9
REPRODUCTIVE ORGANS OF OPUNTIA FULGIDA.
The reproductive structures (flower, fruit, and seed) to which most atten-
tion has been paid in this study, will be described in some detail under three
captions: (1) the origin and structure of the flower; (2) the fruit, its
structure, jxirsistence, and fate, normal and almorraal ; (3) the seed, its
structure, persistence, and germination.
The most aberrant features of the development of these reproductive
organs are : the structure of the wall of the submerged ovary, with its numer-
ous axillary buds ; the capacity of these buds to initiate secondary flowers,
either immediately before the primary ones are open or later, in the same or
succeeding seasons ; and finally the ability of these same axillary buds, when
the fruit is detached, to form adventitious roots and shoots and thus to
initiate new plants.
ORIGIN AND STRUCTURE OF THE FLOWER.
The primary flower of the season in Opuntia fulgida arises from one of
the upper or more terminal axillary buds or areoles of a last year's vegetative
joint or from an areole of a fruit of the first, second, or third year preceding.
The number of flowers developed on any one joint or fniit in a single season
ranges from 1 to 5 or more (figs. 4, 9a). In the case of the fruits, flowers
may be formed from other areoles in succeeding years until as many as 10
or 12 flowers and fruits are often found attached to a single pei*sistent fruit
(fig. 48). The primary flowers of a season are first evident, in 0. fulgida
growing near Tucson, during the latter half of April. Open flowers are
rarely seen before the middle of May. The first flowers to appear and to
open are those developed on vegetative branches. In early May 1912, the
larger flower-buds on vegetative branches of one plant observed were 21 mm.
long, while the longest ones on a persistent fruit of the same plant were but
7 mm. New flowers continue to open successively all through the summer
up to the middle of September. (See Tourney, 1898 ; Lloyd, 1907 ).
DEVELOPMENT OF THE WALL OF THE OVARY WITH ITS TUBERCLES.
The very young flower-bud, when firet pushing out of the tuft of trichomes
and spicules of the areole, is a rather hemispherical body about 0.3 mm.
in diameter. Its dome-like or somewhat conical upper end is fonned by the
few earlier of the 15 to 30 or sometimes 40 leaves that are finally developed
from the Avail of each ovary (figs. 4, 9a, 47). These leaves, w^hen first
fonued, arch over the dome-shaped growing-point (figs. 13, 14). As the
flower grows, the earlier leaves are pushed outward by the younger ones
arising between them (figs. 17, 22). The axis of the flower becomes elon-
gated to 1^/4 times its diameter and its surface becomes very irregrular.
Below each leaf and its associated bud the surface of the wall of the ovary
protrudes to form a prominent tubercle or mammilla (figs. 14, 16, 20). This
tubercle is at first finger-like ; later it projects farthest at its upjier end and
10 THE FRUIT OF OPUNTIA FULGIDA.
narrows to nothing at its lower end, giving it thus a rather triangular outline
in a radial section of the fruit (figs. 4, 17, 28).
At the time of the opening of the flower these tubercles are from 6 to 10
mm. in length, are 4 or 5 mm. wide, and project 2 or 3 mm. at the top. In
the younger flower-bud the radial width of the tubercle is greater in propor-
tion to its length, longitudinal to the ovary, than is indicated above, while in
the mature fruit the projection is much less. In morphological nature, this
tubercle of the opuntias, as has been sho\vn by Goebel (1889, p. 79), is the
combined product of the growing upward together of the leaf-base and the
axillary bud above it. This is clearly indicated by a comparison of different
stages in its development (figs. 12, 14, 15, 17). The upper end of the
tubercle is somewhat circular in cross-section (figs. 30, 49), and somewhat
raised at the margin (figs. 21, 22 ; cf. also, Wetterwald, 1889, fig. 19). At
the highest point of the abaxial side of the margin is borne the leaf, while the
most depressed central portion of the end of the tubercle is occupied by the
flattish growing-point of the axillary bud, which is surrounded by the rudi-
ments of trichomes, spicules, and nectaries developed from it (figs, dl), 12,
15, 32, 50). It is difficult to see how all the structures above a, at the left of
the growing-point in figure 50, can be regarded as parts of a single leaf, as
they apparently would have to be if the view of the morphology of the
tubercle held by Darbishire (1904, p. 395) were accepted.
The growing-point of the flower, like that of the vegetative shoot, may be
slightly convex in form during the period of the initiation of the wall of the
ovary with its tubercles and the leaves borne by them. It may even retain
some of this convexity during the initiation of the 16 or more sepals and
petals (figs. 12, 13, 14), With the beginning of formation of the stamens
and carpels, however, the same growing-point becomes depressed to form a
cup narro^^ing in at the upper margin, about which the numerous (250)
stamens are initiated. Later still, the margin closes in to form the carpels,
which unite above to f oi-m the roof of the ovary, and finally stretch upward to
form the style and its 6 stigmas (figs. 15, 16, 17).
STRUCTURE AND FATE OF THE LEAVES OF THE OVARIAN WALL.
The leaves of the wall of the ovary are, as noted, about 15 to 40 in number.
Each leaf is approximately conical in form, has a slightly flattened base, and
is curved inward above to end in a sharply pointed tip (figs. 4, 5, 11, 19, 23,
47). The mature leaf of the ovary is only 3 or 4 imn. long and but 1 or 1.5
mm. in diameter. It is abruptly constricted at the base to a stalk, which is
nearer the ventral side and is barely a third the diameter of the part of the
leaf just above (figs, 19, 50). The leaves of the lower third of the ovary
do not attain more than half the size mentioned, while those of the upper
quarter, which are more or less appressed against the sepals, may be some-
what longer and are commonly very much broadened (figs. 23, 47, at right).
Before the ovary has reached half the size it attains at the opening of the
THE FRUIT OF OPUNTIA FULGIDA. 11
flower, the lowermost of tlie 15 to 40 leaves of the ovary have dropped off,
many of them withering while mere rudiments, half-grown or less (fig. 20,
lower areole). The separation occurs at the constriction mentioned, and by
the time the flower is well opened all its leaves outside the calyx have fallen.
This separation is apparently not determined by a definite abscission layer.
The dropping of the leaf is followed by the shrinking together of the short
stump of the leaf-stalk and later by the formation of a protecting scar-tissue
of 15 to 20 layers of corky cells (fig. 14). Evidently these leaves of the
wall of the ovary, being relatively few, small, and transient, are able, like the
similar leaves of the vegetative joint, to play only a very subordinate part in
the photosynthetic work of the plant. They are certainly much less impor-
tant in this work than the abundant and permanent photosynthetic tissue of
the wall itself.
In correspondence with this relatively unimportant photosynthetic work
of the leaf, its internal structure shows little of the characteristic specializa-
tion of an efficient starch-making organ (figs. 45, 46). Stomata are few
and scattered, on the under side of the leaf only. Instead of the character-
istic palisade found in the leaves of most other plants and in the joints and
fruits of Opuntia fulgida itself, we find the whole outer region, especially on
the dorsal side of this leaf, made up of nearly isodiametric cells, among
which are scattered small cells containing calcium oxalate crystals and much
larger cells filled with slime or mucilage. The latter are of the type that
will be described in more detail when we come to the consideration of the
internal structure of the fruit (figs. 45, 46). l^ear the flattened base of the
leaf (fig. 45), five vascular bundles are to be seen in its cross-section, but
only the middle one of these reaches to the tip of the leaf. The subordinate,
lateral bundles are made up chiefly of short, broad, thick-Wtilled elements
which are often oriented transversely to the leaf. The principal (median)
bundle also includes many of these element-s at its upper end, but has a
larger proportion of more elongated tracheal elements in its lower portion
(figs. 45, 56).
AREOLES OR AXILLARY BUDS OF THE OVARY.
By far the most significant peculiarity in structure of the wall of the ovary
in Opuntia fulgida, as compared with other angiosperms, is the presence of
the axillary buds or areoles distributed over its surface. There is one of
these within the leaf, or its scar, at the top of each tubercle, though the basal
ones of each fruit remain very rudimentary and never, as far as discovered,
give rise to any structures other than a few small spicules or an occasional
adventitious root on fruits fallen to the ground. What makes these axillary
buds or areoles of the fruits of prime significance in the life of the plant is
the fact that those at least of the upper two-thirds of the fruit remain active
and each capable of giving rise, on the attached fruit, to a secondary flower
or fruit. Or, if the fruit bo detached from the plant, these areoles may give
rise to adventitious roots and to vegetative shoots, thus initiating new plants.
12 THE FRUIT OF OPUNTIA FULGIDA.
The facts and structures of interest in connection with these areoles are:
their number and distribution, the origin of the growing-point, the trich-
omes, the nectaries, the spines, and the bristles or spicules.
NUMBER. SIZE, AND DISTRIBUTION OF THE AREOLES.
Since there is a bud in the axil of each of the leaves of the wall of the
ovarj, except in the cases of 4 or 5 of the upper ones tkat are appressed
against the sepals, the total number of areoles formed is nearly the same as
that of the leaves. Mature ovaries show from 15 to 35 or (in joint-fruits)
even 40 areoles. But these are not by any means alike in size or in. the
number of organs or organ rudiments present in them. The size varies
from 1.5 to 3 mm. in diameter in flowers just opening, while the areoles of a
three-year old fruit may become 4 or 5 mm. broad by 6 or 8 mm. long ( figs,
4, 8, 47, 49). The areoles of the upper third of the fruit are in general
larger and more complexly organized, while those of the lower third are
usually much smaller and of very simple structure. The former are the
ones most likely, under satisfactory conditions, to develop further. The
lower ones usually grow little after the maturing of the fruit. They gTa du-
ally become depressed more and more deeply into the surface of the fruit,
till they are nearly buried from sight. The lower half-dozen areoles have
never been seen to give rise to either flowers or vegetative branches. Tn a
fallen fruit, however, adventitious roots may push out the upper border of
such a dormant or apparently dead areole (fig. 100).
As seen from without, the mature areole appears as a grayish yellow,
bulging cushion, of circular or somewhat longitudinally elongated outline
(figs. 4, 8, 47). The surface of this cushion is made up of the ends of
hundreds of spirally striated trichomes, which at first surround and overtop
all other rudiments in the areole. In slightly advanced areoles dozens or
scores of straight, barbed bristles or glochidia push from beside or beneath
the tuft of trichomes in the apical half of the areole. ITear the middle of
such a cushion may be seen the flattish tops of one or several spine-tipped
nectaries (figs. 14, 47, 48, 49, 50). Still later, in certain of the areoles of
the upper third of the ovary, the tip of the bud of a secondary flower may be
seen. This is at first covered by a protecting lattice made up of the peg-like
leaves, which push out of the cushion of trichomes, just below the crescentic
group of spicules and just above the nectary or nectaries of the areole (figs.
13, 15, 47). In the lower areoles of some of the more elongated fruits one
or two spines may be formed which resemble those found in the areoles of the
vegetative joints, but are usually weaker (figs. 13, 28).
ORIGIN OF THE GROWING-POINT OF THE AREOLE AND THE ORDER OF
INITIATION OF ITS ORGANS.
The growing-point of the areole becomes distinguishable at a time when
the subtending leaf has attained less than a quarter of its mature length;
that is, when it is only 0.5 mm. long. It at first consists of a very small
THE FRUIT OF OPUNTIA FULGIDA. 13
gToiip of more darkly staining cells, located in the very axil of the yonng
leaf (fig's. 12 at x, 14 at x\ 16). With the further growth of the base of
the leaf the supjiorting portion of the stem and the tissue derived from the
axillary bud itself together push outward and upw-ard (see Goebel, 1889, p.
79) to form the young tubercle or mammilla (hgs. 14, 15, 50). This com-
binati(m structure gTOws more rapidly on the outer side, with the result that
the grownng-point of the areole comes to lie on the inner face of the tubercle
(fig. 14). This shoot apex forms a slightly bulging dome of about half the
length of the tubercle and facing directly toward the growing apex of the
flower (fig. 14). Later, by the growth of the tissues and organs arising
from the adaxial side of the growing-point, the upper end of the tubercle
becomes directed more outwardly, often at an angle of 45° with the axis of
the flower (figs. 15, 17, 19). The growing-point of the areole from this
time onward faces almost directly upward (figs. 12, 17, 20, 24).
The first nidiments to appear on the growing-point of the new axillary
bud are the monosiphonous trichomes, which arise on the margin next the
leaf. Following these trichomes there appears a nectary and more trichomes,
on tlie same side, and later another series of trichomes on the opposite or
inner margin of the growing-point (figs. 12, 17).
TRICHOMES OF THE AREOLE.
The first organs to be developed in the areole, after the growing-point
itself, are, as noted above, the monosiphonous trichomes. These are
developed in large numbers, scores or hundreds, by the proliferation of
many adjoining superficial cells about the gro^^'ing-point. At first they
appear aroimd half the circumference of the gro^nng-point on the side next
the subtending leaf (figs. 17, 32, 50). Soon afterward others appear, in
smaller numbers, on the side of the growing-point next the main axis.
When still later a group of spicules appears on this side of the gi-owing-point,
and successive nectaries on the abaxial side, both sorts of structures are sur-
rounded, and more or less hidden, by the masses of trichomes developed
about them. The youngest trichomes, when 3 or 4 cells long, are bent over
the growing-point (figs. 10, 50). Later, w^hen they attain their mature
length of 8 or 10 cells, they stand up nearly perpendicularly about the
gromng-point, though they may (especially in the upper portion) become
considerably bent or kinked (figs. 50, 51). The mature trichome consists
of a single row of from 6 to 10 or 12 cells. It is about 10 or 12 microns in
diameter at the base and three or four times this at the top. The basal cells
of the trichome are usually cylindrical, with thin, smooth walls, while the
up^Der 3 or 4 cells are often barrel-shajwd and have thickened, spirally
marked walls (figs. 51, 52). The terminal cell is often oval, with the
smaller end upward. In the older trichomes one or more of the terminal
cells may have fallen off, leaving the hair with a square end, commonly the
open end of an empty dead cell.
14 THE FRUIT OF OPUNTIA FULGIDA.
There can be no doubt that these trichomes serve to protect from des-
iccation the growing-point of the areole and the young rudiments formed by-
it. In other words, they serve the function served by bud-scales, or modi-
fied leaves, in the axillary buds of most woody plants. The number and
length of these trichomes enables them completely to submerge all other
structures in the bud except the nectaries and the full-grown spicules. The
latter protrude for half their length, while the flat ends of the former can be
seen in surface view of the areole, each with a densely packed ring of
trichomes about it that have been crowded aside by the swelling of the
nectary. These clustered trichomes make a more eftective protection also
because of the enlarged, thick-walled cells at the end of each of them. The
lattice-like thickening of these cells enables them to maintain their form and
full size when dried out completely by the desiccating winds of their native
habitat. Whether the trichomes have other functions at any other period
of their existence has not been detennined. None has suggested itself to
the writer as probable in the course of this study.
The final fate of these trichomes has been suggested by what was said of
the breaking-off of the terminal cells. This process is apparently repeated
until the trichome practically disappears ; at least, the older areoles contain
large numbers of decapitated hairs, many of them with only a few of the
basal cells left.
NECTARIES OF THE AREOLE: THEIR DISTRIBUTION AND MORPHOLOGY.
In every areole, soon after the differentiation of its growing-point and the
development of a few score of trichomes, there appears among the latter, on
the side of the growing-point toAvard the leaf, the rudiment of a nectary.
In many of the smaller, basal areoles of the fruit only one or two of these
nectaries may be formed, and these lie close to the sagittal plane of the
areole (figs. 24, 47). In the larger, upper areoles, however, the nimiber of
nectaries may continue to increase with the growth of the areole until, by the
end of the first gro^ving-season, there may be 8 or 10 nectaries present in.
each (figs. 5, 47, 48, 49). As the areole grows year after year on the per-
sistent fruit, the number of living and withered nectaries may continue to
increase till 20 or more have been formed. iRot more than 4 or 5 mature,
living nectaries are present at one time, but a number of younger ones may
be initiated between a mature one and the growing-point before this begins
to shrivel. In the upper areoles of a primary ovary secondary flower-buds
usually appear after but 2 or 3 nectaries have been developed, and these are
soon crowded aside to wither as the secondary bud swells (figs. 47, 49). In
case secondary flowers are not formed from an areole until the second or a
later year, there may be many old nectaries found crowded aside or partially
crushed by the stalk of the enlarging secondary fruit (fig. 14). These nec-
taries were evidently initiated before the flower, since the latter, as we have
seen, involves the whole gi'owing-point of the areole (figs. 10, 12, 14).
THE FRUIT OF OPUNTIA FULGIDA. 15
The youngest stage of tlie nectary seen was a low, conical projection of the
superficial layers of the nieristem among the trichomes immediately beside
(abaxial to) the growing-point of the areole (figs. 12, 50). Very soon a
small vnscnlar strand is differentia tod, just helow the base of the nectary,
which later penetrates a short distance into it (figs. 50, 5G). As the nec-
tary grows it widens somewhat near the top and becomes more or less con-
stricted at the base (fig. 17). When mature, the stalk of the nectary has
alx)ut three-fifths the diameter of its upper half. The top usually has a
small depression with a small tubercle at its center (figs. 17, 20). Some-
times this tubercle develops to a well-marked spine (fig. 23). These facts
clearly indicate, as has been noted by Ganong (1894, p. 59), that the nectary
is homologous with the spines that are so abundant on the joints of many
opuntias, but are often wanting on their fruits. The steady increase in
number of the nectaries is therefore strictly comparable with the constant
increase in number of the spines of the areole of the vegetative joint
{cf. p. 8)._
The epidermis of the mature nectary is small-celled and thin-walled,
except at the top and on the spine or tubercle itself. Here the cells are small
and irregularly compacted and their walls are provided ^Ai\\ a cutin layer
several microns in thickness, which peels off rather readily (fig. 56). The
cells of the interior of the nectary seem to be little differentiated, except for
the occasional trace of a vascular bundle near the base. They are often
longitudinally elongated to 10 or 12 times their diameter and are commonly
pointed at both ends (fig. 56). Most of these cells in the mature nectary
have darkly staining protoplasts and nuclei, but a considerable number of
them are nearly devoid of contents except for a large, stellate crystal of
calcium oxalate.
The mature nectary remains plump and probably active for one growing
season and then, as has been suggested, it gradually withers and dries up to a
shriveled brown rod of scarcely a tenth the diameter of the functional nec-
tary. It is this shriveled mummy that persists indefinitely, year after year,
among the trichomes of the areole (fig. 14).
SPINES OR THORNS OF THE AREOLE : THEIR DISTRIBUTION, STRUCTURE. AND FATE.
"\Mnle spines, to the number of 6 or 8 and of a length of 3 or 4 cm., are
present in areoles of the vegetative joint of Opuntia fuJgida, they are usually
wanting from the fruits {cf. Wetterwald, 1889, fig. 18). When spines do
occur in a fruit there is usually but a single spine in each of only a few of
its areoles (figs. V), 7c). The position of this spine is essentially that of the
first nectary of the more normal fruits ; that is, it stands in the sagittal plane
of the areole, just wathin the subtending leaf.
The structure of these spines may be described briefly here, leaving the
fuller discussion of this and their development for a later paper in which it is
planned to deal more in detail with the stem. The spines initiated on the
fruit seldom attain the size and strength of those on the stem. They also
16 THE FEUIT OF OPUNTIA FULGIDA.
often drop off with the maturing of the fruit, apparently in consequence of
the withering of the base of the spine. The number of spines in the spine-
bearing areoles of the joint-like fruits evidently increases, from year to year,
much as in the areoles of the stem.
Each spine consists of a slender, barbed axis or core and a glistening
white, striated sheath. The surface cells of the core, in the upper half of its
length, project outward and downward at the tip to form the extremely sharp
retrorse barbs (figs. 53, 54). The sheath, which at first covers the whole
core of the spine with a tightly fitting jacket, is made up of several layers of
greatly elongated and very thick-walled cells (figs. 54, 55), As the spine
matures it shrinks in diameter and separates from the sheath. The latter at
the same time contracts longitudinally, so that its tip is punctured by the
point of the spine. Later the basal portion of the sheath splits to several
strips, which are soon folded back on themselves in loops (fig. 53). The
result of this is that the tips, even of spines developed in the greenhouse, are
left naked for several millimeters.
BRISTLES OR SPICULES OF THE AREOLE: THEIR NUMBER. STRUCTURE. AND FATE.
On the inner or abaxial margin of each areole there is a crescentic group
of barbed, yellow, weak-based bristles, which form the only armament of
most fruits of this species. This curved cluster of spicules reaches about
one-third way around the growing-point of the areole (figs. 32, 50). The
tips of the older bristles lie close against the surface of the ovary just above
the areole. Each individual bristle is practically straight, about 50 or 60
microns in diameter and 1 to 1.5 mm. long. The surface of the bristle is
made up of thick, yellow-walled cells 5 to 8 microns broad by 100 microns
long. The outer ends of these cells project slightly outward and sharply
downward to form the characteristic barbs which make these bristles such a
persistent and irritating reminder of an encounter with the fruits or joints
of this cactus (figs. 57, 58). The cells of the interior of the bristles are of
slightly smaller diameter, more elongated, with clear and much thinner walls
(figs. 58, 59).
The bristles are the last of the several types of organs to appear in the
areole. Even the first of them do not appear till scores of trichomes and
one or two nectaries have been developed (figs. 12, 50). The rudiment of
the bristle is not, like that of the trichome, of a single row of cells, but is 5 or
6 cells across when it first pushes out from the growing-point (fig. 56).
The number of bristles in an areole increases with age. At the time the leaf
is shed the crescentic cluster about the growing-point may consist of 6 or 8
concentric rows of 20 to 30 bristles in each row (figs, 32, 50), In the
sterile areole of a four-year-old fruit this number may be double or triple
that just mentioned. When once formed the bristles evidently persist indefi-
nitely unless dislodged by browsing animals or by the development of a
flower or shoot from the areole. The absorption of a growing-point in the
production of such a flower or shoot of course puts a stop to the appearance of
further bristles from that areole.
l^stjih Carollna^t|fe?0i'a'y
THE FRUIT OF OPUNTIA FULGIDA. 17
PERIANTH. STAMENS. STYLE. AND STIGMA: THEIR DEVELOPMENT
AND ABSCISSION.
The order of initiation of Uie organs of the flower is an acropetal one.
The series begins \ntli the fonnation of the peg-like leaves, followed by that
of the areoles, the sepals, and petals, all from the characteristic convex
groA\'ing-point like that of the stem. Then with a change in the growing-
point to a concave, ciip-like shape, tlie series of floral parts is completed with
the initiation of the stamens and carpels, or perhaps we should say with that
of the placentas and o^alles, which are fonned deep in the bottom of the cup
(cf. alsoGoebel, 1886).
The perianth of Opuniia fulgida consists of about 8 sepals, light green in
color, and of a like number of petals, rose-pink in color. These sepals and
petals are initiated about the gro^\'ing-point in the same way that the leaves
of the ovary are, but differ from the latter in the important particular that no
axillary buds are developed at the bases of the perianth members and that
there is no tubercle formed at the base of either sepal or petal (figs. 17, 22,
4Y). In mature structure also the perianth divisions differ strikingly from
mature leaves. Even the sepals are considerably broader and flatter than
the leaves, with more vascular bundles, while the obovate petals are very
broad and have a far more complex, reticulate vascular system than the
leaves (figs. 47, 64). The mature perianth opens after midday (in mid-
afternoon according to Lloyd, 1907). It forms a saucer-shaped flower an
inch or more across. A few days after opening the whole perianth falls
off, set free by the fonnation of a well-defined abscission layer.
The 250 stamens of the flower have filaments about 2 or 3 times as long
as the anthers. Each stamen arises as a dome-like elevation, 6 or 7 cells in
diameter, on the margin of the now concave gTOwing-point (figs. 16, 18).
As the stamens develop they bend inward over the growing-point, the
youngest ones standing nearly at right angles t^ the axis of the flower (figs.
17, 20). Later they swell at the end, as the microsporangia appear, and
gradually become more erect, but not completely so until the flower is open
(figs. 22, 23, 61).
The internal development of the microsporangia is apparently not essen-
tially different from that of the typical angiosperm. The u}>per, older
stamens open first, as they dry out first. The pollen-gi'ains are irregularly
globular, with a yellowish, pitted exine of about 4 or 5 microns in thickness,
and of a columnar or palisade-like sti'ucture when seen in optical section.
The carpels, the last structures of the flower to be formed, are 6 or some-
times 7 in number. This is clearly indicated by the number of nidiments of
carpels initiated around the growing-point, by the number of lobes of the
stig-ma, and by the number of placentas in the mature ovary (figs. 17, 31,
32, 33, 34). No case was observed with 5 carpels, the number found by
Engelmann ( 1887) in the plants studied by him. The first rudiments of the
carpels become evident after about 6 or 7 tiers of stamens have been devel-
2
18 THE FRUIT OF OPUNTIA FULGIDA.
oped ; that is, when there are 6 or 7 stamens, one above the other, on one side
of the growing-point in a single radial longitudinal section (fig. 18). The
carpel rudiment at its initiation is twice as thick as that of a stamen. It
differs, also, in that it almost immediately bends inward above the growing-
point to meet its fellows and thus to complete the roof of the ovarian cavity
(figs. IT, 18, 19). Soon after the tips of the carpels meet they begin to fuse
together along their radial surfaces to form the rather stout style, which
incloses a papilla-lined stylar canal, that is star-shaped in cross-section (figs.
21, 23, 35, 37). The very tips of the carpels, for a length of 3 or 4 times their
diameter, remain unfused and form the stigmatic lobes. These finally
become 1 to 1.5 mm. long and are densely clothed with swollen, sac-like
hairs that serve for the attachment of pollen-grains (figs. 23, 36). Begin-
ning at a depth of 5 or 6 layers inward from the wall of the stylar canal is a
corrugated tube of conducting tissue 8 to 20 or even 30 cells in thickness,
through which the pollen-tube is to push its way (figs. 22, 34, 35). The
slender cells of this conducting layer extend upward to the very base of the
hairs of the pollen-receiving surface of the stigma (fig. 36). At the base of
the style this layer is continued downward as a series of strands reaching to
the roof of the ovary (figs. 22, 23, 24). The mature stigma lobes are con-
tinued outward and downward to form the characteristic 6-rayed or 7-rayed
structure seen in the open flower (figs. 30, 31). The lining of this part
of the ovary wall, down to the uppermost ovules, is covered by slender hairs
protruding into the cavity of the ovary. These probably help to conduct the
pollen-tubes to the micropyles.
Wot only do the carpellary lobes, which are at first transverse, grow
upward after meeting above the depressed growing-point, but they may
also often grow downward somewhat into the ovarian cavity, thus making
the roof of the latter lowest near the center (figs. 11, 21, 61). Transverse
sections of the ovary at this time may show several upward prolongations of
the ovarian cavity, separated from each other by the downward growth of
the carpels at the plane of juncture of the two carpels of each pair. The
impression given by such a section is that of a compound ovary with 6 or 7
separate cavities.
The separation and fall of the perianth, and other parts that fall with it,
is a complicated and rather variable process, as compared with the shedding
of parts in most choripetalous flowers. In about 3 days after the flower has
opened the withering of the sepals and petals has gone so far that all those
of a flower are twisted together into a cone of dry, crisp remnants ; that is,
the parts of the flower do not drop off individually, as usually happens in
choripetalous angiosperms, but the whole series of sepals, petals, stamens,
and in some cases even the style, are cast off from the ovary at once, all
attached to a cup-like common base stripped off from the upper end of the
ovary. This wholesale shedding of the floral parts is accomplished by the
formation of a highly developed abscission layer across the entire upper end
THE FRUIT OF OPUXTIA FULGIDA. 19
of the ovary. The foi-m of this Layer is not a simple transverse plane, but is
that of an inverted cone, usually perforated at the apex. This funnel-shaped
layer of tissue is initiated in cells 15 or 20 layers beneath the surface of the
cup-like upper end of the ovary that bears the stamens, petals, and sepals
(figs. 23, 58, 60, 61).
In a diametric longitudinal section of the ovary this abscission layer
usually starts in at the base of perianth, either outside the sepals or, more
rarely, between these and the petals. From here it extends downward,
parallel to the surface of the cup at the top of the ovar^^, to a level just a
little above the base of the style, where the abscission layer again comes out
to the surface of this cup (figs. 23, 24, GO, 68). Less frequently the more or
less developed abscission layer may extend across beneath the bottom of the
cup at the top of the ovary. In this latter case the style is cut off, along with
the stamens and perianth attached to the same complete, shriveled funnel
(fig. 61). In the more usual case, first noted, the perianth and stamens only
are borne on a shriveled funnel that is perforated at the base, while the style
is shed separately, breaking across just above its base (fig. 24). In rarer
cases, where the abscission layer starts in at the top within the perianth (fig.
23), the i-)etals and sepals must evidently be cut off separately. Whether a
real abscission layer is developed in each part or not was not determined.
The first origin of the abscission layer across the top of the ovary is evi-
denced by a swelling, chiefly a radial elongation, of a continuous layer of
cells in the midst of the wall of the ovary, in the region stretching between
the base of the perianth and the base of the style (figs. 61, 68). Apparently
any cells along the line of the abscission layer to be may take part in its
formation, except such specialized cells as those of the vascular bundle, the
mucilage cells, and the crystal-holding cells. The cells that are to form
the abscission layer increase in radial length to about twice their tangential
diameter. Then the cells divide tangentially into two nearly isodiametric
cells (figs. 67, 68). A further tangential division follows very soon in each
of these cells, resulting in the formation of a row of 4 cells, of which the two
middle ones have only half the radial thickness of the two outer (fig. 67).
It is at this stage, or sometimes after one or two further tangential divisions,
that abscission occurs. The details of possible changes in the radial walls of
tlie abscission cells have not been studied. (See Lloyd, 1914, p. 70, and
1916, pp. 213-230). It is clear, however, that in consequence of the shrink-
ing of the perianth, on drying, the delicate radial walls of the thin, tubular,
cambium-like cells in the middle of the abscission layer are niptured. The
separation occurs first at the base of the perianth and continues do-v\mward
until the whole top of the ovary, bearing perianth and stamens, and clasping
the style within, curls together and droj)s ofi^ the flower on the second or third
day after its opening. The surface left at the top of the ovary after the
shedding of the periantli shows cleaidy that the break tiikes place in one of
the thin cells in the middle of the abscission layer, and also that it occurs
in the radial wall rather than as a split between two tangential walls (fig.
20 THE FRUIT OF OPUNTIA FULGIDA.
62 ) . Whether or not there is a preliminary softening of the cell-walls of the
abscission layer, there is evidently a change in the cell-walls of the vascular
bundles in the line of fission, as these become flabby and distorted before
abscission occurs (fig. 68). Mucilage cells lying in the line of fission are
usually not traversed by it, but cells within or without these become trans-
formed into abscission cells (figs. 61, 68).
The lining of the funnel left at the toj) of the ovary after abscission is thus
made up, from the outer edge of the funnel do^vn nearly to its bottom, of the
thin-walled cells derived from the abscission layer. Immediately after
abscission the outermost cells dry and shrivel (fig. 62), while cells just below
the surface begin the production of the protective layer of cork cells which
will be noted in describing the fruit (fig. 63). The very bottom of the
funnel left after abscission is in most cases formed by the short stump of the
style, which is apparently cut off by an irregmlar transverse rupture of the
cells without the formation of any distinct abscission layer. The wall of the
funnel for a millimeter just above the stump of the style is still lined by the
epidermis (fig. 24). Only in those cases where the abscission layer cuts
across below the base of the style (fig. 61) is the corky lining of the funnel
complete from the start.
MORPHOLOGY OF THE OVARY.
The flower of this species of Opuntia, like that of any angiosperm, is to be
regarded as a branch of the shoot which bears carpels, stamens, petals, etc.,
instead of the usual photosynthetic leaves, but it is unusual, or indeed almost
unique, in retaining a large series of the characteristics of the vegetative
shoot. This is indicated clearly by certain features of its earlier develop-
ment, by the occurrence on it of photosynthetic leaves with axillary buds, and
by the occasional presence on it of spines, like those of the vegetative shoot.
Further evidence tending in the same direction is offered by the persistence
and secondary growth of the fruit, by the vegetative multiplication of the
flower and fruit, and, finally, by the occurrence of many types of structures
intermediate between the tjq^ical fruit and the typical vegetative joint. In
this assemblage of peculiarities the flowers of this and certdiin allied
opuntias are unique, so far as I can learn from published records. In the
allied genus Peireskia the primary flower does, it is true, bear several pairs
of green leaves, "udth buds in their axils, and 2 or 3 of these may give rise to
secondary flowers. Tertiary flowers, however, are more rare, as far as I
have learned, and clusters of more than 3 or 4 mature fruits have not been
seen. ISTo record has been found of these axillary buds of the ovary giving
rise (either before or after the separation of the fruits from the plant) to
vegetative shoots of the sort formed by fruits of Opuntia fulgida. In the
genus Cereus also something of the same kind evidently occurs at times.
Thus Harris (1905, p. 535) describes briefly the occurrence, in a specimen
of Cereus hoxaniensis, of " several teraiinal fruits, one of which had other
flowers developing from the side." A section of one of the (primary ?)
THE FRUIT OF OPUXTIA FULGIDA. 21
fruits showed it to be sterile. No information is given conceniing the
presence of axillary buds on the primary fruit, though it is clear that these
must have been present to initiate the secondary flowers.
The nearest approach to this structure of the wall of the ovary in these
CactacesB of which I find record in any other family is seen in the genus
Calycanthus. In this form the greatly developed floral axis is depressed at
the top to form a cup, from around the edges of which arise the perianth
members and the stamens. The numerous distinct carpels, on the contrary,
are developed from the bottom of this cup and remain surrounded by it, but
do not play any part in roofing it over, as the carpels of the Opuntia flower
close above its concave growing-point. The outer wall of the cup of this
fruit of Calycanthus bears the scars of many fallen petaloid floral leaves,
distributed much as the leaf-scars and areoles are over the fniit of Opuntia
fidgida. A study of the development of the flower of Calycanthus shows,
however, that there are no axillary buds above its leaves. There is not even
the smallest recognizable rudiment of this, and hence no possibility of the
development of secondary flowers or shoots from the wall of the flower or
fruit.
The facts of development and structure suggested in the paragraph before
the last, together with those detailed earlier in this paper, furnish important
if not conclusive evidence regarding the morphological nature of the ovary of
this opuntia. To the writer these facts seem to offer very strong evidence
for the view that the flower of the opuntias consists of a shorter or longer
vegetative joint, into the depressed upper end of which the ovary is com-
pletely submerged, and around the margin of which the stamens and
perianth members are inserted. This view has been advanced in more or
less definite form by various workers on the Cactacea; in the past. (See
Schumann, 1894, p. 168; Zuccarini, 1844; Toumey, 1905, p. 235; Harris,
1905, etvC.) The evidence for this view, however, has hitherto always
seemed somewhat inadequate. Since it is felt that the present study offers
the most complete chain of evidence thus far produced, especially from the
developmental standpoint, this evidence will be stated here in some detail.
In the first place the external structure of the ovary at the time of opening
of the flower is very like that of a vegetative joint, having prominent mam-
milla?, each of them bearing a conical leaf and a bud in the axil of the latter,
and (rather rarely) a spine like those of the stem itself. As stated above,
the ovaries, and the fruits formed from them, differ markedly in length and
breadth. Thus, the basal part of the ovary may sometimes be short, witli
relatively few mammilla? and areola^, and so give rise to a nearly globular
fruit in which the ovarian cavity reaches nearly to tlie base (figs. 11, 24, 26,
27). In other cases the basal portion of the ovary may be far more
developed, with 20 or even 30 tubercles, and the ovarian cavity may occupy
only the upper third or fifth, or even less, of the portion of the whole floral
joint below the perianth (figs, lb, 28). lu these extremely long flowers the
22 THE FEUIT OF OPUNTIA FULGIDA.
surface of tJie ovary at the base may be much more stem-like than at its upper
end, having more prominent tubercles and furnished with areolae that not
infrequently bear a spine or two each. ISTot only do the real functional
flowers and f iiiits differ considerably in size and in the relative development
of parts, but the semblance to the stem may go so far that the perianth fails
to open, or even fails to develop completely, or (in extreme cases) the carpels
or ovules or even the ovarian cavity itself may never be initiated at all.
Perhaps the small, smooth joiutlets or pseudo-fruits mentioned by
Toumey (1905, p. 531) are to be regarded as the final members of this series
of simplified fruits. These pseudo-fruits occur in more or less dense, fruit-
like clusters, which Toumey says are particularly abundant in adverse sea-
sons, when true fruits are less abundant. Such structures resemble true
fruits in the lack of spines and in the less marked tubercles, but differ in
having no trace of a flower or a perianth scar at the terminal end.
These joints (intermediate in character between flowers or fruits and
normal vegetative joints) occur still more frequently in the allied species
Opuntia leptocaulis, in which practically all degrees of reduction of the
floral parts can readily be found. Perhaps as complete a series could be
found for 0. fulgida after long search, but the intermediate types are far
more abundant in 0. leptocaulis (figs. 89, 96). In the platopuntias also
joint-fruits quite similar in character to those of 0. fulgida are not really
infrequent where large numbers of these plants can be examined in the field.
The stem-like character of these joint-fruits is still more clearly indicated in
these forms, because the normal joints are flat, while the fruits are usually
barrel-shaped or obconcial. A nimiber of examples of these unusual fruits
of the flat opuntias have been mentioned in the literature, chiefly on plants
growing in greenhouses. Most of these abnormal structures have rather
typical perianths, sporophylls, ovarian cavities, etc., but the wall of the
ovary, instead of being as usual a radially symmetrical structure, grows out
on two sides to wing-like expansions. This gives the whole structure the
appearance of a disk-like vegetative joint with a thicker ovary embedded in
its upper margin. This ovary may be at the very top or down more or less
on the lateral margin of the disk.
Secondly, the intenial structure also of the ovary of Opuntia fulgida is
essentially like that of the vegetative joint. Thus the organization of the
areole, the photosynthetic system, and the vascular-bundle system are alike
in the two structures, except for the additional vascular branches supplying
the perianth and sporophylls of the flower (fig. 28).
A third feature in which the fruit of Opuntia fulgida resembles the vege-
tative shoots of the same plant is in its ability to persist for some years on
the parent plant and to continue to grow in thickness year after year by a
well-defined cambium layer. This point is dealt with in more detail else-
where (see p. 29).
Fourthly, the capacity mentioned elsewhere for self-propagation by the
attached flower and that of shoot-production by the fallen fruit are still
THE FRUIT OF OPUNTIA FULGIDA. 23
other features in which these structures resenihlo the v('<;ctativt'. joints of the
shoot.
Fifthly and lastly, the whole history of development of the flower and
fruit, when compared with that of the vegetative shoot, shows clearly that the
whole lower portion of the ovary, up to the perianth, is developed by a convex
growing-point, in every respect just as a branch of the stem is. It is evident
that if the growing-point of a flower, when once initiated, continues its activ-
ity but a short time before the members of the perianth are laid down, the
ovary of that flower will have only a short vegetative portion, and the ovarian
cavity will occupy a considerable portion of the whole length of the ovary
(figs. 23, 25). If, on the contrary, the growing-point that is to form a
flower continues longer to form leaves, areoles, tubercles, etc., there may be a
long stretch of vegetative axis developed Ijefore the perianth and sporophylls
are initiated. Thus the ovary proper may occupy but a small portion of the
upper end of the whole segment or joint which is the product of the continu-
ous activity of this individual gromng-point (figs. 7b, 1c, 28).
The comparison of figures 17, 19, 22, and 23 shows clearly that the ovary
of this cactus is really secondarily submerged by the upward and inward
growth of the portions of the axis just below the perianth. The result of
this growth is that the ovarian cavity, at first formed on a level with the
uppermost areoles (figs. 16, 17), is buried more and more deeply by this
growing upward and rolling inward of the parts of the wall of the ovary that
were laid do^vn before the cavity of the ovary had appeared. This ditfer-
ential growth, which, during the ontogeny of the organ, buries the originally
nearly superficial and terminal ovarian cavity, until it lies near the middle
in the older flower and fruit, suggests clearly the probable phylogenetic
origin of the type of fruit found in this opuntia.
A very striking feature of shoot development in these opuntias is the
marked constriction usually formed at the limits marking the growths of the
same growing-point in successive seasons. This corresponds, of course, to the
boundaries marked by the winter bud-scale scars on the shoots of woody
dicotyledons. The anatomical reasons for this constriction in these opuntias
are not entirely clear. Apparently the protective structures formed about
the terminal bud of the annual shoot at the end of the growing-season render
the tissue here firm and incapable of swelling out in the follo^ving spring to
the thickness of the middle portion of this shoot.
The characteristic origin of the flower in the cylindropuntias is also, as
we have seen, from a new axillary bud which develops a flower with its longer
or shorter ovary in the same season that it pushes out of the areole. In cer-
tain rare instances in Opuntia fulgida, 0. spinosior, and in others seen in
0. cylindrica, growing at Del Monte, California, the part of a flower-forming
joint, containing the ovarian cavity, was marked off from the basal portion
only l)y a veiy slight narrowing of the joint. Such structures seem to indi-
cate that the same growing-point may sometimes develop continuously either
24 THE FRUIT OF OPUNTIA FULGIDA.
during the same season, or more probably for two successive seasons, forming
a vegetative axis in the first and a flower and fruit in the second. This at
least is the most plausible explanation that suggests itself of the origin of
such structures as those shown in figures 7c and 88, where nothing but a very
slight constriction separates a well-developed fruit from a vegetative joint of
the usual length of a yearns shoot.
This same sort of change in the nature of the product of a growing-point,
either between the beginning and end of the same growing-season or in suc-
cessive seasons, will probably prove to be the explanation of the origin of
certain combination joint-fruits found in the flat-jointed opuntias.
The most interesting problem concerning the development of joint and
fruit in these cacti is, of course, that of the cause determining that, up to a
certain stage in the history of the gromng-point of each flower-rudiment,
there shall be formed photosynthetic leaves, tubercles, and areoles only, while
beyond this point the course of development is so changed that thereafter
nothing but floral structures are laid down about the margin of this identical
group of initials. The fact that this change in the character of the rudi-
ments produced on the growing-point occurs at different times in different
flowers of the same plant seems to indicate that the conditions controlling
this are somewhat local in nature. Such experimental attempts as were
made to change the fate of the structures organized about the growing-points
of very young flowers, by removing the persistent fruits bearing these young
flower-buds, gave no clue to the cause or nature of the change in character of
these rudiments. These experiments did, however, show that when the
change has once occurred the character and fate of these buds of the areoles
are not reversible. In other words, if a fruit of Opuntia fulgida is plucked
in February or March and placed in moist sand, certain of its areolesi
will give rise to vegetative shoots. If, on the contrary, the fruits were picked
and planted in April, after the floral structures have been initiated, these
same areoles wither without giving rise to any permanent structures {i. e.,
shoot-buds) such as would have been formed by these very same areoles if
picked a few weeks earlier. Further experiments are being undertaken in
the hope of discovering the material or responsive basis of this change.
It would seem, then, that we have strong evidence, from its structure and
development, for believing that the present type of fruit in Opuntia has
arisen from an originally superior ovary which has progressively sunken
more and more into the upper end of the joint bearing it. However, as
Harris (1905) has pointed out, there is as yet no adequate evidence for con-
cluding with Toumey (1905) that this submergence has occurred very
recently in the phylogeny of the genus or family. It is still possible, of
pourse, that Opuntia is a less-modified type of a series of which Cerev^,
Echinocereus, and Echinocadus are more highly evolved members. In the
latter genera the wall of the ovary may bear numerous bract-like leaves
resembling those of the opuntias and often also bear axillary areoles, having
more or less abundant trichomes and in some cases one or several spines.
THE FRUIT OF OPUNTIA FULGIDA. 25
THE FRUIT: ITS STRUCTURE. PERSISTENCE. AND FATE.
NORMAL AND ABNORMAL.
The fruit of Opuntia fidgida occurs, as we have seen, in ehisters of from a
dozen to a hundred or more depending from one vegetative joint or even, from
a single parent frnit (figs. 2, 3). The individual fruit may he globular in
form, or barrel-shaped, pear-shaped, or still more elongated and nearly cylin-
drical (figs. 3, 4, 7, 26, 28). It may have a diameter of from 20 to 35 mm.
and a length of from 25 to 65 mm. Its size differs with the plant and with
its position in the cluster. The terminal and younger fruits are usually
smaller, but sometimes those of any one growing-season seem small through-
out. The surface of the upper or terminal end of the fruit is formed by the
cork-covered scar left by the fall of the perianth and stamens. This scar is
decidedly concave when young, but with age it flattens out or, in some
cases, even bulges slightly at the center (figs. 3, 25, 28). The lateral sur-
face of the fruit when young has markedly developed tubercles, or mammil-
lae, each terminating in a leaf-scar and its accompanying areole (figs. 4, 17,
31, 32, 47). These tubercles become less prominent as the fruit grows
older and at last nearly disappear, though traces of them are seen in the
pentagonal or hexagonal form, in cross-section, of older fruits (figs. 3,
26, 43).
The internal structure of the fruit is far more variable than that of the
exterior. It may have no seeds at all or it may contain anywhere from 1 ta
200 or more seeds. These seeds may all be shriveled, partially developed
rudiments, or from a few to most of them may possess normally matured
embryos. The number, condition, and structure of the seeds seem to show
no correlation with the external form of the fruit (figs. 25, 26, 28).
The most striking peculiarities of the fruit of this Opuntia are, as
suggested above, its failure to ripen, its persistence on the plant, its long-
continued gi'owth, and finally its capacity for proliferation, whether left
attached to the parent plant or torn loose from it.
THE FRUIT AT THE TIME OF ABSCISSION OF THE PERIANTH.
With the dropping from the ovary of the stamens and perianth we have
left the earliest stage of the fruit proper. Externally, the fruit so formed is
a globular or obconical structure, with a very deep, funnel-like depression in
the top and from 15 to 40 strongly raised tubercles on its sides. Each of the
latter bears a leaf-scar and a more or less developed areole at its upper end,
which was mentioned in describing the ovary of the flowers.
In internal structure this young fruit consists of the superficial epidermis,
which is soon continued over the leaf-scars and perianth-scars by a corky
periderm. Below the epidermis is the 4 or 5 layered hypodennis, consisting
of an outer layer of crystal-holding cells, and within this of 3 or 4 layers of
collencliymatously thickened cells, in which the cell-cavity is finally to be
nearly obliterated (figs. 71, 72). Within the hypodermis are the elabor-
26 THE FEUIT OF OPUNTIA FULGIDA.
ately ventilated, photosyntlietic palisade of the cortex, with its scattered
slime-cells and crystal cells, and the complexly reticulated vascular system ;
and, finally, within the latter and between its meshes are many layers of
mucilaginous storage parenchyma. The latter in turn surrounds the cavity
of the ovary, now nearly filled by the young seeds and by the mass of loose
tissue arising from their long, coiled, funicular strands (fig's. 23_, 40, 71).
The somewhat uneven outer layer of the epidermis of the projecting
tubercles consists at this stage of rather cuboidal cells, with bulging and
considerably thickened outer walls (fig. 71). The epidermal cells of the
gTooves between the tubercles are somewhat elongated radially and thinner-
walled than those of the outer margins of the tubercles just described.
Stomata are scattered rather frequently over the surface of the tubercles.
The guard-cells are already sunken considerably below the surface, though
not as far as in the mature fruit (figs. 71, 72). The inner layer of the epi-
dermis already includes many crystal-containing cells of the sort figured in
detail in the older fruit (fig. 71, 72, 73).
The cork of the fruit at this stage is confined to the pit-like scar at the
top of the fruit, where it forms an ashy-white layer. It consists, outside the
phellogen, of above 8 to 10 layers of rectang-ular cells approximately 100
microns long and broad and 20 to 40 microns thick, radially. The walls of
all save one layer of these are not greatly thickened, nor apparently strongly
suberized (fig. 63). The very bottom of this cup around the stump of the
style is commonly still protected only by the original epidermis, which, as
was noted earlier, is often not cast off along with that part of the lining of the
cup which bears the stamens (figs. 23, 60).
The photosynthetic tissue of the ovary-wall has already beg-un to assume
the striking arrangement in radial rows that is so characteristic of the
cortical tissue of the mature fruit as well as of the vegetative joint (figs. 39,
70, 71, 73). Scattered abundantly through this palisade, which extends
inward 8 or 10 cells from the surface, are numerous mucilage-cells of the
usual more rounded form.
The vascular-bundle system of the young fruit consists of about 16 pri-
mary bundles entering it at the base. These soon divide by dichotomous
forking to form twice as many biuidles at the level of the lower end of the
ovarian cavity. The repetition of this forking gives rise in the upper half
of the fruit to a still more complex system of main vascular bundles (figs.
17, 21, 25,26). From the points of forking of these main bundles are given
off the groups of smaller bundles, one group at the base of each tubercle, to
supply the tubercle, its growing-point, and the leaf and nectaries arising
from it (figs. 21, 27, 28, 32). The main vascular bundles are nearly isodia-
metric in cross-section at this stage of development, and are about 500
microns thick radially and 300 microns broad tangentially (fig. 44a). In
internal structure, which may be noted briefly for comparison with the
bundle of the older fruit, each main bundle includes about 25 or 30 tangen-
THE FRUIT OF OPUNTIA FULGIDA. 27
tial layers of xjlem elements. Outside of these lies a group of 6 or 8 layers
of radially arranged cambium-cells and their little modified derivatives.
Still further outward on the same radius is the half-cylindrical strand of
phloem-cells, about 15 to 20 cells thick radially (fig. 44a). From a ring
of anastomosed bundles near the rim of the funnel at the top of the fruit
a series of downward-growing branches gives rise to the 6 or 7 pairs of
placental bundles, one pair running longitudinally behind each double row
of ovules (figs. 11, 22, 23, 26, 28, 38, 39, 41). From this same vascular
ring numerous small branches grow inward and upward. These are the
ones that supplied the stamens and perianth members before they were shed.
Other similar branches grow still farther downward and then turn upward
to form the 6 or 7 bundles of the style and stiginas (figs. 20, 22, 23, 28, 37,
41,61).
The most important structures within the fruit — the seeds — arise, as we
have seen, in a double row on each of the 6 or 7 placentae. There are from 8
to 12 or more young seeds in each row, making from 100 to sometimes 200
or more seeds that are initiated in the finiit as a whole. Usually not all of
these mature. Sometimes, as noted above, none of them mature. At the
time the perianth is dropped there is a decided difference in size among the
seeds present in any one ovary. The most developed are about 0.5 mm. in
diameter inside the pocket of the funiculus in which each seed is inclosed
and about 0.25 mm. thick. The seed-coats are unthickened and have only
2 layers of cells each. The embryo sac has usually reached the 8-nucleate
stage. The cavity of the ovary is at this time about half filled with the seeds
and the swollen funiculi or seed-stalks.
THE MATURE FRUIT.
At the end of the growing-season, which in Tucson terminates about the
middle of October, the fruit has attained what must be regarded as a mature
stage. The seeds within it are now full grown. These mature fruits, of from
3 to 5 months' growth, differ considerably in shape and size. They are
commonly pear-shaped, or somewhat more rounded, and have a diameter of
12 to 15 mm., with a length of 20 to 35 mm. or more (figs. 3', 7, 8). Later
fruits of the season may be as large as, or even larger than, the earlier ones.
Fruits of one season may average in all dimensions larger than those of the
season before.
The surface of the typical fruit at maturity has filled out so that the
tubercles have lost their prominence. The areoles differ in size on the same
fruit, the upper or larger ones at this time being 15 to 30 or even 35 mm. in
diameter. Occasionally an elongated fruit will be formed which has much
the appearance of a mammillate vegetative joint, except for the presence of
the perianth-scar at the top and the fact that the spines are weaker than in
most joints (fig. 7).
The most important features of the internal structure of the fruit are those
concerned with the vascular bundles of the wall of the ovary and with the
28 THE FRUIT OF OPUNTIA FULGIDA.
character and contents of the ovarian cavity. The main vascular bundles of
the wall increase only moderately after the fall of the perianth, though they
do increase somewhat in radial dimensions by the addition of new layers of
xylem tissues (fig. 44&). The amount of the cortical parenchyma outside
the vascular bundles may also increase somewhat, and this latter growth is
probably the cause of the rounding out of the fruit and the disappearance of
the mammillse (figs. 3, 76, 8).
The number and character of the seeds present in different fruits differ
markedly. There may sometimes be an ovarian cavity filling three-fifths of
the diameter of the fruit, or this cavity may be practically wanting. About
half the mature fruits contain one or more ripe seeds, which vary in number
from 1 to 100 or 200 per fruit. The other half of the fruits have only small
ovarian cavities in which the seed rudiments have ceased their development
at different stages from half-formed ovules up to half -grown seeds (fig. 23).
In some cases not even these withered rudiments can be found in the place
where the ovarian cavity should be.
A consideration of the facts related inclines at first to the conclusion that
ovaries mature into fruits only when pollination has occurred and that seeds
form only when the further process of fertilization has taken place. This
seems doubtful, however, in view of the fact that many seeds may go half-
way through their development before degeneration sets in. The attempt is
being made to determine the distribution of these different types of degenera-
tion in different plants and different flowers of the same plant.
The most striking peculiarity of these mature fruits is that they do not
ripen. From analogy with all other fruits, we should expect at this time
that the flesh of the Opuntia fruit would either change color and soften or
harden up to form a dry fruit. But nothing of this sort happens. The
matured fruit, with its color still bright green, with its photosynthetic tissues
still active in starch-making, and its well-established fascicular cambium
simply halted until the next spring, enters into the resting-period of 4 or 5
months. There is not the slightest sign of ripening or any change at all
comparable with this process. There is no preparation of any sort for the
discharge or escape of the seeds to conditions conducive to germination.
On the contrary, the majority of the mature fruits normally remain attached
to the parent shoot, not merely through the succeeding fall and winter, but
season after season for several or many years. These persistent fruits
become essentially a part of the vegetative shoot, performing not only the
photosynthetic function of a vegetative joint, but also budding out new
shoots. Usually these shoots arising from attached fruits are floral shoots.
More rarely a vegetative joint may arise from such a fruit, and then the
latter becomes a constitutent joint of the vegetative branch, undistingiTish-
able except by its perianth-scar and usually by its lack of spines (fig. 79).
The fate of a fruit in these respects is the same, whether it contains many
fertile seeds or whether, as may often be the case, it is entirely seedless.
THE FRUIT OF OPUNTTA FULGIDA. 29
THE PERENNATING FRUIT: ITS STRUCTURE AND SECONDARY GROWTH.
The matured fruits of Opuntia fulgida not only do not ripen at the end of
the growing-season, but (as noted above) they are neither shed from the
plants as most fruits are, nor do they open in any way to discharge their
seeds. On the contrary, these fruits remain year after year, attached and
actively growing, until they may become 40 or 50 mm. in diameter and 70
or 80 mm. long. The growth of these fruits in length must be chiefly
primary ; that is, each fruit attains practically its maximum length during
its first season's growth. Thus the longer fruits mentioned must have been
exceptionally long at the start.
Growth in thickness of the larger fruits is, on the contrary, largely
secondary. It is accomplished by the persistent activity of the fascicular
cambium and by the general multiplication of the parenchyma cells between
the bundles. Whether there is an increase in the central medullary
parenchyma of the fruit has not been determined with certainty, but
there appears to be some little increase in the interior diameter of the
vascular ring. The cortical parenchyma, inside the hypoderm, may in-
crease in thickness from about 2 mm. in the just-matured fruit to 5 mm.
or more in a fruit several years of age. This radial growth seems to be
almost entirely a result of the radial elongation of the cortical cells, as the
number of these along a radius ranges from 20 to 25 in both the just-matured
fruit and in that 3 or 4 years old.
The fascicular cambium of the perennating fruit gives rise to numerous
phloem and xylem elements, which increase the radial dimension of the
bundle from O.Y or 0.8 mm. in the newly matured fruit to 3 or 3.5 mm. in a
fruit several years old. The radial extent of the xylem in the newly formed
fruit is about 0.6 mm. and that of the phloem 0.2 mm., while in an older
fruit the dimensions are 2.6 mm. for the xylem and 0.6 mm. for the phloem.
This shows that the growth of the two tissues has kept their bulk much the
same relatively. The tangential growth of the bundles is relatively slight,
the outer edge of a bundle 4 or 5 years old being only half as wide again as
that of one in the first-year fruit. ISTo definite annual rings could be dis-
tinguished in the wood of these older fruits. The number of larger xylem
elements along a single radius in a young fruit is about 25, while in a 4 or 5
year fruit there may be 80 or 90 vessels on a single radius.
The parenchyma of the pith-rays differs from that of the cortex by show-
ing a vigorous cell multiplication. The pith-ray of the just-matured fruit
may have but 8 or 10 cells in the radial extent of the bundle, while in a
fruit 4 or 5 years old a pith-ray may be made up of 25 or 30 cells in the
radial width of the bundle. This growth is apparently due to the general
division of cells throughout the ray, as no trace of an interfascicular
cambium is discoverable.
Two structures only on the surface of the fruit undergo important changes
as the fruit ages. These are the corky periderm and the areoles. At the
30 THE FRUIT OF OPUNTIA FULGIDA.
end of the season of its origin the fruit is protected by the well-cutinized
epidermis and the underlying hypodermis, except for the perianth-scar and
the individual leaf-scars. This epidermis persists over the general surface
of the fruit for several years. Only where the epidermis is cracked by the
swelling of the fiTiit or is otherwise injured is the original protective layer
replaced in function by cork, like that of the perianth-scar.
The periderm of the perianth-scar has its origin, as we have noted, from
a pliellogen layer arising in descendants of the original cells of the abscission
layer, just within the plane of abscission (figs, 62, 63). The first 5 or 6
layers of cork cells formed by the cork cambium are very thin-walled ; then
there is formed a single layer of very thick cells (see Wolfe, 1912, figs. 6,
7, 9). These sclerenchyma-like cells have walls of a pale-yellow color,
which in older fruits are made up of from 15 to 20 distinct layers marked by
numerous minute radial pits (figs. 63, 64, 65). The walls stain intensely
with safranin and gentian violet. The cork cambium, after forming this
thick layer, may continue to form more thin-walled cork cells until, in the
older fruits, 12 to 15 or more layers are present inside the intact, thick layer.
These later layers are more numerous on the upper margin of the perianth
scar. With increasing age the 5 or 6 layers of thin cork outside the scleren-
chyma layer, which are left more or less shriveled after abscission, are grad-
ually worn off from the more exposed parts of the scar. This leaves the
sclerenchyma as the superficial and essentially protective layer unless this is
injured. When this primary sclerenchyma layer is broken a secondary one
is formed immediately outside the then active phellogen (fig. 14, at right).
Periderm formation in the region of the areole begins soon after the fall
of the leaf, in an area that includes tissue of the leaf -scar itself and a few
of the epidermal cells below and beside this (fig. 14). There is thus formed
a periderm of from 3 or 4 to 8 or 10 cells in thickness, of which the portion
immediately above the foliar bundle may finally include 3 or even 4 immedi-
ately superposed sclerenchyma layers (figs. 63, 64). As development of the
areole proceeds the cork layer develops upward from the leaf-scar and
thin-walled cork-like but apparently little-suberized cells are formed imme-
diately beneath the persistent trichomes, just above the leaf. Later the
formation of these cells continues on beneath the bases of the withered nec-
taries and spines if there are any, and finally beneath the bristles (figs. 14,
17). The latter, in older fruits, may be supported upon 12 to 15 or more
layers of clear thin-walled cork-like cells (fig. 14). The only parts of the
areoles that are not covered are the growing-point and the immediately sur-
rounding series of rudiments of nectaries, bristles, etc. These all lie well-
protected at the base of the dense tuft of younger tricbomes that overhang
the growing-point (fig. 50).
On the lateral surface of the older fruit corky tissue may arise by the
extension of the cork about the areole, or that of the perianth-scar over the
edge of the cup,' or it may arise de novo from injured spots in the clear epi-
THE FRUIT OF OPUNTIA FULGIDA. 31
dermis between the areoles. In this way considerable portions of the sur-
face of a fruit 4 or 5 years old may become covered with cork developed
below cracks or bruised spots, and the fruit thus come to have the mottled
green and gray color characteristic of maturing vegetative joints (fig. 3).
The effect of this cork, aside from affording protection to the water-stored
cortical tissues, must be also to cut off the light and air from the photosyn-
thetic cells of the portion of the fruit covered by it. While lessening its
starch-making capacity, the cork is thus of prime importance to the fruit in
maintaining it as a supporting and conducting structure for the flowers and
persistent fruits that may arise from it year after year.
The structure of the areole in the young fruit has already been discussed
(p. 12). The chief change in the areole with increased age of the fruit
is the increase in size, until it may become 3 or 4 mm. broad and 6 or 8 mm.
long in the case of those near the top of the fruit. This increase in size is
due chiefly to the continued production of hundreds of trichomes year after
year. These appear in rather definite concentric circles around the growing-
point. Besides the trichomes, the areole also forms additional nectaries,
year after year, till at least a score may successively develop and wither.
The bristles of the fertile areole, as has been noted, are not increased in num-
ber after a flower is initiated (figs. 14, 17, 50). The sort of development
here indicated is the characteristic one for many of the areoles of the upper
half of the ovary throughout the life of the fruit. Others of the basal half
or quarter of the fruit may persist, but show only slight growth for 2 or 3
years and then cease growing altogether.
Other of the upper areoles, several in each fruit, give rise to one or the
other of the two most important structures developed from fruits. These
are the floral shoots that may arise on the attached fruit and the vegetative
shoot that develops from the areole of a detached fruit. These structures
are, of course, the normal products of axillary buds. Hence the earlier
period, during which these areoles are developing only modified structures
like bristles and nectaries, must be regarded as a sort of resting-period in
which the normal activity of the bud is inhibited.
When the normal development of an areole is accomplished and a shoot
produced, all further activity by this areole is terminated, as must be evident
from the fact that the whole mass of the single growing-point of the areole is
embodied in either the vegetative shoot or the flower. The exact conditions
conducive to the production of a flower in one case and a vegetative shoot in
another, with the details of development of each, will be described, as far
as kno^\Tl, in the discussion of proliferation (see pp. 35-50).
The possible activities of the fruit of Opuntia fulgida may be summarized
as follows: The fruit usually remains attached and in succeeding seasons
buds out new flowers. If fruits fall to the ground from increasing weight
of the cluster or when dislodged by wind or brow^sing animals, then any one
of three things may happen. Most frequently the fruit dries up or decays
32 THE FRUIT OF OPUNTIA FULGIDA.
and nothing comes of it. If it drops on moderately moist soil, then it may
give rise to roots and shoots bv proliferation from the areoles. More rarely
still, the fruit may set the seeds free by decay and the latter may possibly
then germinate to seedling plants. This latter fate, which must be regarded
as the most normal one for such a fruit, is evidently a very rare one for the
fruit of Opuntia fulgida, at least in the deserts near Tucson, v^^here seedlings
have never been seen.
THE SEED: ITS STRUCTURE, PERSISTENCE. AND
GERMINATION.
The ripe seed is the one essential structure of the fruit which remains
entirely unchanged year after year, as the fruit persists on the parent plant.
The mature or ripe seed is an irregular, round-angled, flattened disk about
5 mm. in diameter and il.5 to 2 mm. thick in the middle (fig. 77). It usually
bulges on both sides of the disk, but often far more on one side than the
other. The majority of good seeds are pale yellow in color, with remnants
of many colorless cells from the fleshy ovule-stalks sticking to them. In
internal structure the seed consists of a well-developed curved embryo bent
in the plane of the disk-like seed, of a small remnant of endosperm near the
center of the seed and embraced by the bent embryo, and finally of a protect-
ing j acket, formed chiefly by the layers of tissue arising from the pocket of
the funiculus, but including also the two thin integuments (figs. 76, 77).
The embryo is from 0.7 to 1 mm. in diameter and about 4 or 5 mm. long.
It is bent in the plane perpendicular to that of the adjacent faces of the coty-
ledons. Most of the cells of both cotyledons and radicle of the embryo are
densely stored with what appear to be aleurone grains and slime globules.
These bodies take on a brownish and not a bluish color with iodine, and
show structural features not characteristic of starch-grains. Occasional
cells of the cotyledons and upper part of the radicle are completely occupied
each with a large cr^^stal of calcium oxylate like those found in the paren-
chyma of the mature plant.
The endosperm, which consists of a small mass in the bend between radicle
and cotyledons and of thinner layers extending along beside the radicle and
over the tips of the cotyledons (fig. 98), is densely stored with starch which
reacts in the usual way with iodine.
Small fragments of perisperai, left in the corners where the embryo fits
the integument less accurately, are filled with granules reacting like those in
the embryo itself. The cell-contents of both embryo and endosperm seem to
remain entirely unchanged in fruits that have persisted on the plant for
many years after the maturing of the seeds. The integuments are made up
of considerably thickened cells, the outermost layer of them with w^avy
brown walls.
The jacket derived from the funiculus surrounds the seed completely,
having finally closed in above the micropyle (fig. 97). It makes up more
THE FRUIT OF OPUNTIA FULGIDA. 33
than nine-tentlis of the thickness of the coat surrounding the seed and con-
sists of three distinct layers. The inner layer is from 150 to 300 microns
thick. It consists of intertwisted threads or fibers which run meridionally
about the seed. The component cells of these threads are 8 to 10 microns in
diameter each by 150 or 200 microns long. The middle layer of the funi-
cular pocket is made up of somewhat similar interwoven threads running
equatorially, i. e., around the luargin of the disk-like seed. The cells of this
layer are 20 to 25 microns in diameter, but only 50 to 60 microns long. The
third or outermost layer of the seed-coat is very uneven, consisting of a single
layer of cuboidal cells 30 or 40 microns thick, about most of the margin of
the seed, but of Y or 8 layers with a total thickness of 400 microns on the
sides of the seed. It is this greater thiclmess of the outer funicular layer
that makes up most of the bulge on the flat side of the disk-like seed.
The whole structure and condition of the seed apparently remain quite
unchanged year after year so long as the fruit containing it remains attached
to the tree. Not only are the embryos of seeds from the oldest attached
fruits still plump, with the stored starch intact, but a seed from such an old
f niit is just as capable of germinating as one from a fruit just matured.
A very important question arising in this connection is : Why do not
these seeds, immersed in the moist pulp of the parent fruit and raised each
summer to a relatively high temperature, germinate there, without waiting
to escape from the fruit ? The attempt was made to germinate seeds under
these conditions by treating them in the manner which was found necessary
to secure germination outside the fruit, that is, by chipping the seed-coat.
Seeds with the coats cut off at one edge Avere carefully inserted in the pulp
of sound fruits witli every precaution not to injure the fruit more than neces-
sary. The wound was then sealed with vaseline and set in a moderately
moist chamber to induce germination. No germinations of seeds under
these conditions were secured. In each case, whether the injured fruit
dried out, decayed, or took root in the soil, the embrj^o of the inserted seed
after some weeks blackened and died. The explanation of this failure of
the seed to germinate in its oavh fruit or in the host fruit was not discovered.
It is, of course, possible that it may be found in the mere exclusion of oxygen
by the seed-coat or by the mucilaginous pulp of its OA\m or the host fruit.
On the other hand, it is quite possible that the osmotic or chemical character
of the cell-sap of the pulp surrounding the seeds is the real obstacle to
germination.
During two sojourns at Tucson the attempt was made to test the common
report that seedlings of Opuntia fulgida do not occur in the field about
Tucson (Tourney, 1905, p. 360). Diligent search was made for them in
many groves of these trees in the months of April and May of 1912 and
1915, but not a single imdoubted seedling of this species was discovered.
Examination of large numbers of fallen fniits showed no sign of germina-
tion of the seeds. It then occurred to the writer that a search on a cattle
3
34 THE FRUIT OF OPUNTIA FULGIDA.
range outside the protected, ungrazed property of the Desert Laboratory
might show that seedlings arose from seeds that had passed through the ali-
mentary canals of cattle that had eaten the fruits. This search also proved
futile. It is of course possible that seedlings may occur in other parts of
the area of distribution of this opuntia, or in the Tucson region itself, at
other seasons.
With the hope of discovering something regarding the cause or causes of
this failure of the seeds to germinate naturally, the attempt was made to
germinate them artificially. In the first place, dozens of plump seeds likely
to possess good embryos were repeatedly, in spring, autumn, and winter,
sown on soil or on filter-paper, and put either in a warm gi'eenhouse or on a
warm bath at 30° to 35°. 'Not a single germination was obtained from
these experiments.
Other series of somngs were made of plump and apparently fertile seeds
from which the seed-coat had been cut or filed away at one part of the
margin. Out of several dozens of these cut seeds so^m between layers of
damp filter-paper in a gallon battery-jar, only about 8 or 10 germinated.
The best proportion of germinations obtained was 5 embryos out of 25 prob-
ably fertile seeds.
The difficulties in determining what proportion of seeds are capable of
germination are two. In the first place, it is impossible to tell from its
external appearance whether a seed has a normal, well-developed embryo or
not. Quite aside from the half -developed and withered seeds, there are
many of mature size, and apparently plump and healthy, which upon being
cut open reveal no embryo at all, or a discolored and shriveled one with no
stored material in it. Secondly, of the seeds that are cut into far enough
to determine whether they contain good embryos, or far enough to make
certain the escape of the swelling embryo from within, some may be so
injured as to prevent germination of any sort.
The trials made thus far show that a certain relatively small percentage of
the seeds of this opuntia are fertile and capable (if aided in getting out of the
coat) of producing normal seedlings (fig. Y6).
THE FRUIT OF OPUNTIA FULGIDA. 35
PROLIFERATION OF FLOWERS AND FRUITS.
The most unique peculiarity of the flower or fruit of Opuntia fulgida is
its ability to produce new shoots. These shoots may be floral shoots only,
as in the case of the attached flower or fruit, or they may be vegetative shoots,
as in the case of detached fruit. This capacity for proliferation is depend-
ent, as has been noted, on the presence and persistence of the axillary buds or
areoles of the wall of the ovary. These axillary buds are unknown, as far as
the writer has been able to leam, on the ovary of any other family of plants,
and even in the Cactacese occur only in the genera Opuntia, Nopalea, and
Peireskia.
The structure of these areoles, with a description of the rudiments present
in them, has already been noted (p. 11). We have seen also that most
of the areoles of a flow^er and fruit may persist year after year without
developing anything but minor organs,- such as nectaries, trichomes, and
spicules. We have now to consider the very important function perfoiined
by certain of the areoles in their proliferation to shoots of limited or
unlimited growth. There are three types of proliferation by the areoles of
the ovary of this opuntia. In the first place, from 1 to 5 or more of the
areoles of the unopened flower may give rise to the buds of secondary flowers,
which open soon after the primary ones. Secondly, one or several areoles of
an attached fruit may in the first or in some later season after its develop-
ment give rise to primary flowers of that season. Thirdly, the areoles of a
detached fruit that has been separated from the parent plant after maturing
and placed on moist soil may give rise, first to adventitious roots and then
later to the characteristic joints of vegetative shoots. The fruit thus per-
forms the unique function of initiating a new plant by purely vegetative
propagation.
PROLIFERATION FROM ATTACHED FLOWER BUDS.
The primary flowers of the season arise in either April or May on either
the vegetative joints or the fruits of the preceding season or sometimes on
those of a still earlier season. These flowers are developed from the growing-
points of the upper areoles of the joint or fniit (fig. 47) in the manner noted
above (p. 9).
Before the primary flower is half-grown the buds of secondary flowers of
various sizes can be detected developing in from 1 to 4 or 5 of its upper
areoles (figs, ^a, 9&, 13). By the time the primai-y flower is ready to open,
soon after the middle of May at Tucson, the larger buds of the secondary
flowers are about one-sixth grown, and are recognizable as buds of flowers
rather than of vegetative shoots (figs. 9a, 9&, 47). About 4 weeks after the
primary flower withers and sheds its perianth, the largest secondary flower in
its turn opens. This occurs usually between the middle and end of June,
and the buds of the tertiary flow^ers are then already well developed in their
36 THE FRUIT OF OPUXTIA FULGIDA.
upper areoles. In the latter part of July flowers for the fourth generation
of the season are developing from the areoles of the tertiary ones (fig. 6).
These quaternary flowers probably open during August, and since the
blooming-season may extend into September (Lloyd, Plant World, 1917), it
is probable that a fifth generation of flowers may be formed in a single
season. 'No undoubted examples of this, however, have thus far been seen,
and I have not been able personally to seek them at Tucson at the proper
season.
Since the fruits resulting from the four generations of flowers remain
attached to each other in the order of their development, it is clear that a
chain of fruits of at least four successive linlvs may be developed in a single
season. This has been recorded by Toumey (1898), who apparently
believed that all chains of fruits arose in this way in a single season. He
definitely mentions that the " proliferous fruit hangs in pendulous clusters,
sometimes as many as 7 fruits in a single cluster, one growing from the other
in continuous succession." Pie regards the persistence of fruits over winter
and the formation of flowers from them in the succeeding spring as a rare
occurrence.
The time of maturing of the seeds of the fruits of the four successive gen-
erations may differ considerably, since the fruits continue to grow after
dropping the perianth, but even the latest and smallest ones may contain
ripe seeds in October. All four links of the chain may commonly persist
attached throughout the winter and give rise to new flowers the following
spring. ISTot infrequently, however, the younger, quaternary fruits may
wither more or less during the winter and (failing to develop flowers upon
them in the succeeding spring) may be crowded off by the new flowers
developed beside them on the tertiary fruit by which they themselves are
borne.
The formation of these chains of fruits of four links in a single season
is thus the result of the continuous uninterrupted development of the grow-
ing-points of certain areoles of each successive floral shoot. The structure
thus formed is comparable with that developed by many herbaceous plants
and the water-shoots of certain woody ones, in which each (or many) of the
axillary buds develops continuously during the season of its initiation into a
mature vegetative or reproductive shoot.
Other areoles of the flower and fruit of this opuntia have quite an opposite
fate. In these the axial bud does not develop continuously, but ( after devel-
oping a considerable number of trichomes and spicules and a few nectaries)
rests till the next growing-season, or sometimes for three or four seasons,
before renewing its development.
THE FRUIT OF OPUNTIA FULGIDA. 37
PROLIFERATION OF PERSISTENT ATTACHED FRUITS.
While certain of the upper areoles of a flower may, as we have seen,
develop at once into secondary flowers which open soon after the primary
one, other areoles of the same or another flower may practically cease growth
with the opening of the flower and persist over one or more winters as resting
buds. These buds, retaining their capacity for further development, may
give rise, in the succeeding or a later spring, to the primary flowers of
that season (fig. 4, 7c). Such flowers may arise from any of the 4 or 5
younger fruits of a chain (fig. 4).
The development of these flowers, arising from resting buds of persistent
fruits, is identical with that of flowers arising from the areoles of flower-
buds, and the fruits formed in the two cases can not be distinguished. The
flowers arising from fruits, just as those from the areoles of unopened
flowers, may give rise in turn to buds of secondary flowers, and these to ter-
tiary and perhaps quaternary ones in the same season. The repetition of
this process of budding out flowers from fruits and then flower from flower
several times each season, when repeated season after season, results finally
in the formation of fruit clusters of great size. Clusters of 20 to 30 fruits
are common, and clusters of 100 or more fruits of all ages suspended from a
single parent fruit are not rare (figs. 2, 3). Some of the longer chains may
embody 12 or 14 generations of fruits in a single chain (fig. 77). Since, as
we have seen, certain of the links added in any one season may wither and
fall off, it is evident that a chain of 12 generations of fruits does not repre-
sent merely the growth of three seasons, 4 fruits per season, but may repre-
sent the product of five or six seasons ; in fact, the size and appearance of
some of the basal fruits of these clusters indicates an age of more than 6
years. The records of the effect of exceptionally cold winters on the plants at
Tucson show that it must often take many seasons to build up a chain of 12
or 14 links. Thus, in the winter of 1912-13 there was an exceptionally hard
freeze, soon after which great numbers of the younger persisting fruits fell
off the trees, so that chains of more than 3 or 4 links were hard to find.
Such a periodic shortening of the chains, even if it occurred but once in
three or four winters, would increase considerably the number of summers
necessary to produce chains of fruits of the total length of the longer chains
found.
The ease with which these fruits may be set free from the plant will be
the more readily realized when we note the very slender stalks by which the
heavy fruits are attached (figs. 25, 26). These stalks also, especially in the
younger fruits, have little lignified tissue. Jarring of the tree by A\T[nd or
by broAvsing cattle, which eat many of the fruits in dry seasons, may shake
off numbers of fruits that are often found strewn thickly beneath larger
plants. The stalks of the older fruits, on the contrary, become steadily
thicker and stronger, and the upper ones are thereby enabled to hold the
heavy clusters that hang from them.
38 THE FRUIT OF OPUNTIA FULGIDA.
PROLIFERATION OF FALLEN FRUITS.
If the fruit of Opuntia fulgida remains attached to the tree the only struc-
tures produced by its areoles are trichomes, nectaries, and flowers. This is
practically universally true. Among many hundreds examined, only two
cases were seen in which a vegetative shoot had arisen from an attached
fi-uit. If, however, fruits are plucked from the tree and placed on moist
soil, there arise from their areoles not flowers but roots and later vegetative
shoots, and so new plants are initiated ; that is, if any given fruit remains
attached there may arise from the growing-point of a certain areole a rela-
tively short shoot which develops leaves and axillary buds, but soon ends its
activity with the formation of a set of stamens and carpels. If the same
fruit were detached the same areole, and thus the very same growing-point,
may give rise to a shoot of unlimited growth, while other areoles near the
soil form adventitious roots. This production of new plants from buds on
the wall of the ovary in the fruit is a surprising phenomenon ; in fact, it is as
unique as the formation of flowers from axillary buds of the ovary of
the unopened flowers.
This process of the vegetative sprouting of a fruit planted in soil to a new
plant often occurs in 50 to 75 per cent of fruits planted in the greenhouse.
In the field about Tucson, at least in the spring of the year, it occurs but
rarely. A careful examination of some scores of young plants of this
species, of 3 or 4 joints in height, in the desert near Tucson, in May 1915,
showed that all had arisen from fallen vegetative joints. ISTone of the fallen
fruits seen at this time showed any preparation for the development of new
plantlets. This is the more surprising because the soil had been considerably
moistened that season by unusually copious rains. In September, however,
a careful search by an assistant, B. R. Bovee, revealed a few very young-
plants which had evidently arisen from fallen fruits. It is possible, there-
fore, that under some conditions, such as those existing during years of
favorable summer rains, a considerable number of new plants may thus arise
from fruits.
The origin of new plants from rooted fruits will be described as it has been
observed in the greenhouse. The process is clearly the same in the field, as
far as could be seen from the few plantlets found there. Many different
plantings of the fruits were made at Tucson in April and May, at South
Harpswell in July and August, and at Baltimore in February, October, and
December, These all gave substantially the same results, in spite of the fact
that the Tucson plantings were of fruits that would in a week or two have
produced flowers if they had been left on the parent plant, while those
planted in Baltimore had entered into the resting-stage for the winter (figs.
78,99).
Fruits that are half -buried in a soil that is kept moist but not saturated
may begin to form adventitious roots within the first week. In 5 weeks' time
the fruit has been found fastened securely in the soil by several roots, some
THE FRUIT OF OPUNTIA FULGIDA. 39
of them 5 cm. long, 1 mm. thick, and often branched several times. These
roots arise chiefly on the buried portion of the fniits and always develop
from an areole, from the broken surface of the fruit-stalk, or more rarely
from near the edge of the perianth-scar. From this statement it will be
seen that roots may arise at either the basal or apical end of the fruit, or
at both, depending on whether the fruit is laid horizontally or whether one
end is placed lower in the soil. My observations do not confirm the con-
clusion of Toumey (1905) that the " roots appear chiefly at the basal end of
the fallen joint." Though the roots arise from the areole, they do not arise
from its growing-point, in the middle of the areole, but from the still active
tissue around its edge. Very often a root pushes out above the cluster of
bristles on the adaxial margin of the areole, but a root may rise also from
any other part of the margin (fig. 100). One or several roots may arise
from the same areole. When a root is developed from the scar of the fruit-
stalk it is usually from its margin. As such a root matures, however, the
vascular bundles of the root soon come to form continuations of the bundles
at the base of the fruit. When a root develops on a perianth-scar it appears
always to originate in the region of the cork cambium, and it breaks through
the cork itself in emerging (figs. 78, 99, 100).
The initiation of a shoot by a detached fruit does not occur until some
time after the first roots are developed on it. The formation and function-
ing of roots are apparently necessary antecedents to shoot formation. In
fruits planted in the greenhouse at Tucson on April 26, kept well watered
and at rather high temperatures, shoots began to push out of some areoles by
May 25, and on the following September 10 all but one or two of the 18
fmits planted had one or more vegetative joints on it. Some of the latter
were 2 cm. long. Similar results, though not so universally successful, were
obtained from plantings at South Harpswell and Baltimore. One lot of
fruits planted at Baltimore produced shoots only 3 or 4 cm. long in a year ;
while others, with more soil, had shoots 10 cm. long in five months.
One or several joints may arise from each fruit, either simultaneously or
successively. They may arise from areoles on the exposed surface of the
planted fruit or sometimes from those joints at the surface of the soil, but
nearly always from the larger areoles of the apical half of the fruit. This is
without regard to whether the fruit is planted on the side, -with apex down,
or with the base do\\ai.
The shoot arising from the areole of a fallen fruit is formed by the grow-
ing-point of the areole, just as a flower is, or just as a branch is from a vege-
tative joint. The new shoot, however, is for a long time dift'erent from the
branch of a mature plant in remaining slender and in the permanent delicacy
of its spines (fig. 78). In fact, it has the appearance of one of the early
joints of a seedling. The primary shoot, as developed in the greenhouse in
Baltimore, usually does not branch until the second season. Quite early in
its development the new shoots, especially if it has arisen near or under the
40 THE FRUIT OF OPUNTIA FULGIDA.
soil, sends down adventitious roots of its own which soon become an impor-
tant part of the root-sjstem of the new plant.
From what has been said of the slow development of plantlets from
sprouting fruits in the laboratory, it is evident that it takes a number of
years to develop a mature flowering plant from a fruit. It is doubtful
whether such a plant can mature more than a year or two sooner than a seed-
ling started at the same time.
Examination of plantlets, from sprouted fruits and also of those from
fallen joints, shows that not all of the fallen fruit or joint enters into the
make-up of the first or basal joint of the new plant. The portion which does
so probably depends in part upon the position in which the fruit falls, or is
planted, on the soil and on the relative positions on the fruit of the areoles
forming the roots and those forming the shoots. It is a common occurrence
for a part (often a fourth or a third) of the fruit, including both cortex and
vascular bundles, to be cut off by a layer of cork from the part going into
the first joint of the new plant (fig. 99). The phellogen from which this
cork arises is formed by the parenchyma of the cortical and medullary-
tissues.
The fate of the different parts of the vascular system of the parent fruit
has not been followed out in all details, but it is clear that much of the old
system plays no important part in the new plant and that some of it is cast
off with the cut-off portion of the fruit (fig. 99). The chief part of the old
system to do service in the new.plantlet is that which lies most directly
between the point of origin of the adventitious roots and that of the primary
shoot of the plantlet (fig. 99). These strands quickly become thickened to
many times the diameter of the other bundles of the parent fruit. The seeds
present in these sprouting fruits evidently persist indefinitely in the flesh of
the latter. Their ultimate fate has not yet been determined, as the oldest
plantlets seen which were known to be of this origin were but 2 years old.
While roots may arise from parts of the fallen fruit outside the areole,
such as the scar of the fruit-stalk or of the perianth, it is apparently not pos-
sible for shoots to arise elsewhere than from the areole. The experiment
was tried repeatedly of planting fruits, all the areoles of which had been
destroyed by cauterization, to determine whether other superficial tissues
might be stimulated to produce new-shoot growing-points. Though some of
these cauterized fruits took root in the soil and remained plump and green
for 24 months, they developed no visible rudiment of a shoot.
An attempt was made also to determine whether halves or quarters of a
fruit, in which the cut surfaces were either covered with vaseline or dried,
could be made to take root and form new shoots. This was partially success-
ful in only a few instances where part of the piece remained green for a time
and some roots were formed, but in no case was a single shoot formed. This
was due apparently to the fact that a softening and decay of the exposed pulp
of the cut fruit took place, similar to that which occurred in fruits punc-
tured for the insertion of cut seeds (see p. 33).
THE FRUIT OF OPUNTIA FULGIDA. 41
Finally, attempts were made to determine by experiment whether an
areole that had once borne a fruit could, after careful removal of this, give
rise to a vegetative shoot. When from such fmits all the flowers and sec-
ondary fruits Avere removed, and all other areoles cauterized, and the fruits
then planted in soil, no shoots at all arose from any of their areoles. This,
of course, is rather to be expected, with but a single growing-point in each
areole. But the latter condition had not been demonstrated histologically
at the time the experiment was initiated. Then, too, it could not be assumed
impossible for some of the younger, protected cells from about the margin
of an areole of the primary fruit that had already produced a secondary
fruit to give rise to a new-shoot growing-point, just as cells outside the areole
may initiate a new-root growing-point. In a check experiment 21 fruits
that had borne flowers were planted after the removal of these and no areoles
cauterized. In 10 months one fruit was dead, 21 were living and rooted, and
17 of these bore shoots 3 to 4 cm. high. This demonstrated that no wound
injurious to the fruit as a whole is caused by the removal of the secondary
flower or fruit. On the other hand, the fact that many of the cauterized
fruits mentioned took root and remained green and plump for two years
demonstrates that cauterization does not seriously injure the fruit as a whole.
CAUSES AND SIGNIFICANCE OF PERENNATION AND OF THE
DIVERSE TYPES OF PROLIFERATION.
We have described above the unusual persistence and secondary growth of
the fruits of this opuntia and the entirely unique power of the proliferation
to flowers and vegetative shoots shown by the areoles of its ovary. Beyond
these facts of the structure and habit of fruit and areole lie the physiological
problems of the causes and significance in the life-history of these striking
peculiarities in this species of Opuntia.
The primary question to be answered is: Why does the fruit of this
cactus never ripen like those of most cacti and of the vast majority of other
angiosperms ? ITo appreciable light on this question has been obtained from
a study of this opuntia itself. Not a single fruit of this species has been
seen, not even an abnormal one, that showed any indication of undergoing
those changes which characterize the process of ripening in most other cacti.
The persistence, year after year, of fruits containing mature ripe seeds in
attachment to the parent plant is another peculiarity entirely unexplained
by observation thus far made on this opuntia. Dropping off or springing
open is in the case of most plants a phenomenon closely associated with the
process of ripening. The most noteworthy exception to this general rule is
that of Callistemon and allied Myrtaceje investigated by Ewart (1907),
where the fruits persist almost indefinitely until killed by the cutting off of
the water-supply by fire or drought (fig. 80).
One possible explanation of the persistent greenness and attachment of
the fruit is suggested by the study of an interesting abnormal phenomenon
42 THE FRTJIT OF OPUNTIA FULGIDA.
observed in certain other Arizona opimtias. The most striking case of those
studied is afforded by Opwifia versicolor^ a species in which the normal
structure of shoot, flower, and fruit is quite similar to that found in Opuntia
fulgida.
The fruit of 0. versicolor is quite variable in form, size, and habit as to
ripening and persistence. It may be nearly globular and from 15 to 20 mm.
in diameter, as is true of most of the smaller fruits, or it may be a much-elon-
gated structure whose whole length is 4 or 5 times its diameter (figs. 82, 84).
These fruits do not soften greatly or change color with the ripening of the
seeds, but remain green or yellowish during the autumn and, according to
Tourney (1898), usually ripen, wither, and dry up while still on the tree
during early winter. Some of the apparently normal fruits, however, as
Toumey noted, may remain attached for a year or even two years. This is
demonstrated by figures 82, 83, and 86, which were photogi-aphed in late
April.
On examination of large numbers of these plants of Opuntia versicolor in
April and May, it was found that most of them (about Y5 per cent) bore no
persistent fruits. Of those plants which did bear apparently normal per-
sistent fruits, 9 out of 10 bore abnormal gall-like fruits also, of which we
shall say more presently. It seems possible then, that the cause of the per-
sistence of the normal fruits may be the same as the cause of the abnormality
as well as of the persistence of the far more common gall fruits.
These gall fruits have an exceedingly interesting developmental history.
They seem very clearly to be caused by the deposit in the flower-buds of the
eggs of the cactus fly {Asphondylia opuntice). These eggs may apparently
be deposited at different times in different cases, for the galls show that the
flower bud has been arrested and diverted from its normal course at different
phases of its development. The galls show that in some cases the arrest of
normal development of the flower occurred when the perianth had hardly
been initiated, in other cases after the perianth had been half -formed, and
in yet others not until the perianth was fully developed (fig. 84, a, h, c, d).
The degree of disturbance of the normal development of the internal
organs of the flower differs markedly. In some cases the stamens, pistils,
and even the ovules may have been well started only to become distorted and
withered without maturing, while in others no traces of stamens or ovules
are te be discovered. Quite independent of these internal features are the
size and external form attained by the distorted bud. Sometimes it may be
no larger than some normal buds at the time of opening, while again it may
reach a length and diameter twice or thrice the normal (fig. 84 a, c). In
general external appearance most of these fruits in early April have a plump
green ovary and often dark-red, waxy petals. Many of them, in fact, look
precisely like gigantic, but otherwise normal flower buds that seem just
ready to burst into bloom (fig. 84(i). It is surprising that the petals can
persist all winter and retain a color which though darker than the outside of
THE FRUIT OF OPUNTIA FULGIDA. 43
the petals is not very different from that of the inner surface of the petals in
many flowers of this cactus. A section through such an abnormal flower-bud
gall taken in April shows from a few to dozens or sometimes scores of the
small pupge of Asphondylia within the gall. They are embedded in the
cortical region of the ovary, chiefly in the portion above the small ovarian
cavity, and they stand perpendicular to the surface of the bud.
In spite of the rather normal appearance of many of the flower-buds which
have wintered over unchanged from the preceding season, they never open to
flowers. The nearest approach to this process is found in the curling open
of the tips of the petals as the buds finally wither (fig. 81). The only open-
ing of these galls that does occur is of quite a different sort. During May,
especially in the latter half, the pupse of the cactus fly transform to imagos
and break out through the epidermis of the bud, each independently. The
pupa-cases are left with half their length projecting beyond the surface of
the gall (fig. 81). The fly itself perches on the gall while its wings are
hardening (figs. 81, 84), and then flits off to play its part in infecting the
new flower-buds of the season, which are then just pushing out of the areoles
of the vegetative joints. By the end of May a large share of the emptied
galls have withered and dropped to the ground, where they decay, often by
the aid of fungi, which have ready entrance about the old pupa cases.
We come now to the consideration of the possible relation between the
gall fruits or gall buds and the apparently persistent fruits. As was stated
above, many of these latter fruits contain apparently good seeds. Others
have only withered rudiments of seeds, and thus resemble certain of the
gall fruits. In fact, a complete series of structures can be discovered
grading almost imperceptibly, in both external and internal features, from
typical fruits to a persistent normal-appearing flower bud. This, together
with the fact that the normal type of persistent fruit in 90 per cent of the
cases occurs on plants that also bear gall fraits, suggests that both have a
common cause (figs. 82, 84).
If it is the presence of the egg or larva of Asphondylia or of some sub-
stance deposited with the egg that inhibits the normal development of the
flower, but stimulates it to an abnormal and locally excessive growth and also
causes it to persist over winter, then some lesser amount or degi-ee of this
same stimulus may be responsible for the persistence of the apparently nor-
mal fruits. Such stimulation might occur either by transmission of some
substance or of some stimulus from an infected fruit to a neighboring one,
which had not been infected. It is also possible that a fruit which had been
bored for the deposit of a single egg, or a few, might continue to develop
normally in every respect, except that it persisted on the tree. The only way
to distinguish between these two possibilities would be by experimental
study. The latter of the two \aewt) stated seems supported by the observed
fact that the buds containing most pupa? are generally the ones most modified
in structure, while buds or fruits with few pupse are relatively little
modified.
44 THE FRUIT OF OPUNTIA FULGIDA.
In other species, such as the flat- jointed Opimtia discata, the disturbance
of the normal development of the flower and fruit hj the laying of the eggs
of Asphondylia is never so marked as in Opuntia versicolor. The perianth
of this species is always shed, leaving a definite scar. This probably means
that it develops to maturity and then opens more or less completely. The
general form and size of the resulting fruit are relatively little affected (fig.
87). The ripening of the fniit also is only partially inhibited, though the
complete ripening and subsequent fall of the fruit are rarely accomplished
normally. In one example found at Tucson a fruit of 1913, bearing 50 or
more Aspliondylia scars, persisted and bore a vegetative joint 5 cm. long
in 1914, and both were plump and green when collected in May 1915.
Usually the fly escapes from its pupa-case and the riddled f niit mthers as it
does in Opuntia versicolor.
Griffiths (1913, p. 18) reports that a similar retention of the gall-like
flower-buds or fruits in Opuntia puberula is due to the attack of the black
opuntia louse.
If the explanation suggested above for the retention and modification in
structure of the flower-buds of Opuntia versicolor is the real one for this
case, then it is quite possible that a similar one may be found for the similar
peculiarities of 0. fulgida. That is, it is conceivable that some relatively
slight change or lack of change in the nature of the cell-sap, or in the char-
acter of photosynthetic or other metabolic products of Opuntia fulgida, from
a cause as simple as the sting of a fly, though as yet undiscovered, may prove
the adequate explanation of the peculiarities of the fruit of this cactus.
Experiments have been initiated to test this hypothesis by the aid of injec-
tions and by otherwise changing the external or internal conditions affecting
the plant. They have not yet been completed.
We have still to discuss the marked diversity in behavior, under the same
conditions, of the different axillary buds of the flower or matured fruit, and
also that of the same buds of the fruit under different conditions. If a
mature fruit of Opuntia fulgida is taken from the tree at any time from
October to April and placed on damp soil, some of its areoles will push out
to vegetative shoots. On the other hand, if the same fruit were to be left on
the tree till May no shoots at all would be formed, but the same areoles might
give rise to flowers instead of vegetative shoots. Moreover, while only the
areoles of the distal quarter of the flower or fruit develop so long as the fruit
remains attached, any of the buds, except those of the very basal quarter of
the fallen fruit, may give rise to root or shoot. The areoles which actually
do this are determined by the position of the fruit on the soil. Finally, if
these same fruits are taken from the tree about May 1 and planted, the
areoles which had already begun to swell slightly do not go on to develop vege-
tative shoots, but may either fail altogether to develop or give rise to small,
imperfect flower-buds, which soon wither and drop off. Later, other and
more basal areoles may proliferate to vegetative shoots.
THE FRUIT OF OPUNTIA FULGIDA. 45
The questions we have to answer here are these : Why do areoles of fruits
that are picked and planted in April give rise, in the follovs^ing month, to
nothing but vegetative shoots when if, on the other hand, these fruits were
to be left attached till May the same areoles would give rise in that month to
flowers, and to these only ? Secondly, what sort of change occurs in the
areoles or fruit between April 1 and May 1 which makes the fruit detached
at the latter date incapable of doing what it could do if detached at the earlier
one ? Thirdly, why do none but the most distal buds of a fruit give rise to
flowers, while any but the most basal areoles of a fallen fruit may develop
shoots ?
In regard to the first question, it has occurred to the writer that the
attached fruits give rise to flowers because these fruits and their areoles are
supplied with substances — perhaps flower-forming substances — which differ
markedly from those supplied to the areoles of the same fruit when it has
fallen and become rooted in the ground. Or, perhaps the process of root
formation may itself produce substances that inhibit flower formation in the
same fruit. The plan to experiment on this by rooting attached fruits in
pots of soil supported beneath them in the field has not yet been carried out.
Several attached vegetative joints of a plant growing in the greenhouse at
Baltimore, which from their position seemed likely to produce flowers, were
rooted in pots placed beneath them. In the first season, however, these joints
developed neither shoots nor fruits. It is planned to repeat this experiment
on attached fruits and joints in the field at the first opportimity.
When a good-sized vegetative joint or two consecutive joints bearing sev-
eral fruits is rooted in the soil, these fruits still give rise to shoot-buds only.
This is true in spite of the fact that tlie conditions of nutrition here would be
expected to be more nearly like those of fruits on a growing plant.
It was also attempted to discover by experiment whether the production of
flowers alone by attached fruits is definitely influenced by the amount and
kind of nutritive material available for them, in consequence of their rela-
tion to the vegetative branches bearing them and to other fruits. In each of
4 plants of Opuntia fulgida several branches were denuded of all fruits
except 3 or 4 sets of 1 or 2 fruits each. After three seasons' growth the num-
ber of new flowers and fruits that had arisen from these undisturbed fruits
was not at all abnoraially increased, nor had the treatment induced the for-
mation of a vegetative joint on a single one of the original fruits. The chief
tendency of the new growth in these plants was toward the development of
new vegetative joints from the old, partially denuded ones. This was most
strikingly shown in a tree from which 300 fruits and 100 joints, including
the top of the stem, had been lopped off and only two fertile branches with
small fruit-clusters left. In this tree the new growth consisted almost
entirely of vegetative joints clustered about the cut ends of the main stem
and branches. In these cases, therefore, the diversion of all available nutri-
46 THE FETJIT OF OPUNTIA FULGIDA.
tive material of the vegetative branch into one or two fruits, instead of into
several scores, did not change the fate of the areoles on these fmits. There
was no increase of the vegetative activity in them such as might have been
expected as a result of the increased available food-supply.
In seeking a reply to the second question proposed on page 45 it was
found that all attempts made by planting very young flower-buds to induce
these to become metamorphosed into vegetative shoots were unsuccessful.
The evidence from these experiments seemed to show that when once tha
growing-point of an areole has started, even if but barely started, to form a
flower, it can not be diverted and made to give rise to a vegetative shoot, as it
could by removing the fruit from the plant and planting it a few weeks
earlier. In every case the young flower-bud on a planted fruit either failed
to develop at all or developed but slightly and then withered.
In essential agreement with these results in sprouting the detached fruits
are those observed in detached vegetative joints of Opuntia fulgida. Fallen
joints, as we have noted, very commonly take root and give rise to new plants.
In no case of scores observed were flowers developed from such rooted
joints until after a considerable shoot system had been formed.
In Opuntia vulgaris, however, a series of experiments made in May and
June 1917, gave very different results. In practically every case the term-
inal joint or pair of joints removed just before the flower buds appear, or
just after they are visible, will root promptly and then develop normal flowers
and in most cases set fruit (see Hildebrandt, 1888, p. 110).
The third question raised must apparently be answered by attributing to
the influence of polarity the restriction of flower buds to the most distal
areoles of the fruit. This is very pronounced so long as the fruit is attached,
and is definitely related to the base ; that is, to the point of attachment of the
fruit. In fallen fruits a much less definite polarity is exhibited which is
determined by the points of origin of roots and new shoots.
Another problem suggesting itself in connection with the production of
flowers from fruits is the discovery of the reason for the fact that only the
terminal fruits of a cluster and a few of the subterminal ones give rise to
fruits, while all the fruits basal to these, from 1 to 8 or even 10, produce no
flowers. This seemed to be equally true whether this basal part of a chain
bore one or several secondary or branch chains upon it. In collaboration
with Dr. Hermann Spoehr, who planned the chemical side of the work,
analyses were made of the pulp of the two basal fruits and the two terminal
fruits of each of several chains of six or more fruits. We were unable, how-
ever, to discover any difference in the carbohydrates and other nutrient sub-
stances present in the distal flower-forming fruits and the basal sterile ones.
THE FRUIT OF OPUNTIA FULGIDA. 47
PROLIFERATION OF THE FLOWER OR FRUIT
IN ALLIED SPECIES.
The proliferation of the ovarian wall, either in flower or fruit, has been
noted in a number of other opimtias, and in at least one other genus, by
Engehnaun (1887), Hildebrandt (1888), and a number of more recent
workers. (See also, Penzig, 1890, p. 507). Associated with this prolif-
eration in certain cases we find a persistence of the fruits for one or more
years after maturing. The areoles of the attached fruits of some of these
species are known to form flowers only. The attached fruits of others, on
the contrary, may develop not only new flowers and fruits, but, under certain
conditions, give rise to vegetative shoots also. Of the first type are Opuntia
cylindnca, 0. leptocaulis, 0. catacantha, and Peireskia guamacho Rose.
Of the second sort are Opuntia rufida, 0. spinosissima , 0. discata, 0. versi-
color, and 0. arbuscula.
Opuntia cylindrica, growing under cultivation but out of doors at Del
Monte, California, frequently formed flowers by proliferation from the per-
sistent fruits of the previous season (fig. 88). This same species also fur-
nished striking examples of the development of first a vegetative joint and
then a fruit by the uninterrupted activity of the same growing-point ; that is,
the joint and fruit are separated by only a very slight constriction, as was
noted in speaking of Opuntia fulgida (cf. figs. 7c^ 88). From the plants of
0. cylindrica observed there is no evidence that the primary flowers ever give
rise to buds of secondary ones before they are open.
Opuntia toumeyi, growing near Tucson, may occasionally form secondary
flowers close to the base of the primary ones, which open soon after the latter.
Opuntia leptocaulis is a slender Arizona species, growing along with 0.
fulgida, in which fruits may persist unripened or half-ripened and then
bud out new flowers in the succeeding season (fig. 89, a, h, c). These pri-
mary fruits may persist for a year and a half and the secondary ones may
ripen, but tertiary fruits are rarely formed. The propagative structures
here show a very closely graded series of intenuediatc forms between the
typical fruit and the vegetative joint, a series far more complete than can
usually be found on 0. fulgida or any other near Tucson. One plant of 0.
leptocaulis seen at Chico in August bore numerous slender vegetative
joints on persistent fruits of the same season and also of the preceding season.
The graded series of propagative structures above mentioned contains
typical obovate fruits, with definite perianth-scars, evidently fonned by nor-
mally opened flowers. Other fruits are twice as long, but still show the scar
of a normal perianth. Then there are joints of various lengihs, of wliich
some bear small or very small perianth-scars while others have no scars at
all, and yet all of them look very fruit-like in other external aspects. There,
are also many slender joints having no perianth-scars, yet closely resembling
the more slender sterile fruits that do have them, l^one of these various
structures except the shorter, obovoid ones may contain seeds, and some even
48 THE FRUIT OF OPUNTIA FULGIDA.
of these are seedless. Any of the sterile, fruit-like bodies may be easily dis-
lodged and on moist ground their areoles may give rise to new plants. Such
a complete series of more or less fruit-like structures might easily give the
impression that these sterile propagules have arisen phylogenetically by the
progressive sterilization of the normal type of fruit, accompanied by an
increase in its povt^er of sprouting from its areoles until the sterile fruits
have become the chief propagative structures of this species. The plausi-
bility of this view we shall consider in detail later (p. 52). In the mean-
time, however, we must remember that the so-called fruit of these opuntias
is made up largely of purely vegetative elements, the internodes and the
areoles and their products. It is clearly for this reason that many sterile ova-
ries, such as in other angiosperms (where they occur commonly) would soon
wither and fall, may in Opuntia persist as essentially vegetative structures.
Opuntia catacantha {0. rubescens Salm-Dyck) is a West Indian species
resembling 0. fulgida in certain respects more closely than any other opuntia
studied. It is tree-like, with very flat, paddle-shaped or scimitar-shaped
joints, which in the variety studied are without spines. The fruits persist
from one season to the next and then bear primary flowers of the latter sea-
son. These may bear secondary flowers and the latter form tertiary ones,
and thus chains of fruits consisting of at least 6 or 8 links may finally be
formed (fig. 90). These fruits vary in size, form, and internal structure.
The flowers and young fruits are slender and obconical or sometimes slightly
bent (fig. 90). As the fruits mature they increase considerably in size,
often to about twice the original length (50 to 60 mm.) and to 4 or 5 times
their original thickness. Mature fruits are often flattened until only half as
thick on one transverse axis as on the other (lY by 30 mm. for example, in
one sho\ATi in fig. 9). Few of the fruits have fertile seeds. 'None of those
dissected by the writer had good seeds, but a few ripe seeds were sent him
by a correspondent, the Rev. A. B. Romig, of St. Thomas, Virgin Islands.
The seed remnants found are of various sizes up to about half-growm seeds,
but all are brown and withered. No definite information is available
regarding the ability of these fruits to sprout to new shoots, but the fact that
they are nearly always sterile suggests that they may serve as propagules just
as the fruits of 0. fulgida do. This possibility is rendered more plausible by
the fact that in another spiny variety of Opuntia catacantha (0. monili-
formis Haworth) collected on Mona Islands, near Haiti, by Dr. N". L. Brit-
ton, chains of short joints 1.5 by 3' cm. long are formed, which are said to
sprout to new plants. These are spiny and except in size are like the regular
vegetative joints. They are not pseudo-fruits like those described in 0.
leptocaulis.
In PeiresJcia guamacho is found the most striking case of proliferation of
the flower that has been seen outside the genus Opuntia, and it appears the
more remarkable because of the large bracts and long stalks of the successive
flowers. In this species, as it grows in greenhouses in Washington, each
THE FRUIT OF OPUNTIA FULGIDA. 49
flower usually bears 4 bracts and each of these has a secondary flower in its
axil. The stalks of a secondary flower may get to be a centimeter long or
more and this gives the flower-cluster quite a different appearance from that
of an opuntia, though its general plan is the same (figs. 92, 93). One or
two, rarely more, of the flowers in such a group may develop fruits (cf.,
Delavaud, 1858). Each globular, fleshy fruit bears a well-defined areole
above each bract-scar and usually contains from one to several large, flat
seeds. These seeds germinate readily, but all attempts to induce the areoles
of a detached, unripened fruit to proliferate to a shoot failed. No case of
the vegetative proliferation of the areole of a fruit was observed. In a
similar species of Peireskia growing at Chico, a single parent fruit some-
times bore 5 secondary fruits and the basal secondary ones not uncommonly
bore in turn tertiary fruits ; that is, three generations of fruits were formed
in a single season.
In the second series of species mentioned on page 47 the attached friiit
sometimes proliferates to form vegetative joints as well as to give rise to
flower buds. All but one of these opuntias resemble 0. fulgida in that they
form these vegetative shoots only rarely. Thus, in the flat-jointed species,
Opuntia rufida, from Doctor Rose's collection in Washington, in 0. spinosis-
sima from Jamaica, and in 0. discata, studied in the field at Tucson, the
development of vegetative shoots from attached fruits occurred very infre-
quently (fig. 94). Hildebrandt (1888, p. 112) has reported such a case in a
flat-jointed Opuntia gro\\dng in Freiburg. He attributed this imusual
behavior to exceptionally good nutrition of the cultivated specimens. Pro-
liferation of the fruits I foimd not at all uncommon in a number of the
above-mentioned opuntias, and of other flat opuntias growing in the collec-
tion of Doctor Griffiths, at Chico, California {cf. Griffiths, 1913). In the
cylindrical species, 0. versicolor, the occurrence of such a proliferation of
the attached fruit to vegetative joints is relatively very rare, only 3 or 4 cases
being seen in hundreds of plants examined. In two at least of the three
cases of this tjq^e observed the proliferating fruit was evidently a gall fruit
(fig. 85 ) . This fact of itself proves that these gall fruits do not always drop
off during the second spring. It is doubtful, however, if they are capable,
except in the rarest instances, of holding on long enough to make their vegeta-
tive offshoots an important part of the branch system. The irregularity in
branching, usually resulting from proliferation of a gall fruit to a branch,
should make this phenomenon discoverable several years after its occurrence
(figs. 85, 86). No certain cases could be found, however, that indicated
clearly the persistence of such a fruit-borne branch for more than a year or
two. This sort of proliferation is practically identical with that occurring
so rarely in Opuntia fulgida, except that in the latter the proliferating fruit
is in other res])ects often a normal one.
On the contrary, in the round-jointed Opuntia arhuscula, the proliferation
of attached fruits to form vegetative shoots is, under some conditions at least,
4
50 THE FEUIT OF OPUNTIA FULGIDA.
not a rarity, but a very common occurrence. The fruit of this species is per-
sistently green, shows no sign of ripening, and not more than 5 per cent of
them have well-ripened seeds. This fruit is pear-shaped, rather slender,
smooth, and spineless, like that of 0. fulgida, and has rather prominent
areoles. The areoles of the primary flower very often proliferate to secon-
dary flowers and the fruits commonly persist over one or more winters. Most
of the persistent fruits are single, but chains of two are common and chains of
3 or 4 links are not infrequent. The fruits of the upper part of the rather
bush-like plant seem always to produce only flowers so long as they remain
attached. Many of the fruits of the lower branches, however, often give rise,
from one or more up to 6 or 8 of the distal areoles, to rather slender, con-
densed branches, bearing numerous prominent areoles ( fig, 95 ) . These con-
densed branches, which may also arise on vegetative joints, are vertical in
position, are about 4 or 5 mm. in diameter, and 20 to 50 mm. long. If these
short branches are left on the plant they may thicken somewhat and become
more like the normal, terete, vegetative shoots. ISTo evidence was obtained,
however, that the persistent fruit and its vegetative offshoot ever become
incorporated into the permanent branch system of the parent plant. These
condensed branches apparently play no important part in the development of
this opuntia, except when the fruits or the branches alone fall to the ground,
there to take root and thus start new plants.
Wliat has been said of the proliferation of the fruits in the various
Opuntias and in Peireskia indicates that each is peculiar in its own way in
regard to the ripening of the fruit, in its persistence, and its proliferation to
flowers or to vegetative shoots.
In the first place, the fruits of two species, 0. arhuscula and 0. catacantha,
have fruits resembling those of 0. fulgida in that they normally fail
to ripen. The other four species, 0. cylindrica, 0. leptocaulis, 0. rufida,
and 0. versicolor, apparently fail to ripen only because of some unusual
condition within or about them.
Secondly, of the .eight species of Opuntia just mentioned only two, 0.
arhuscula and 0. catacantha, seem to resemble 0. fidgida in having normally
persistent fruits. In the others this is the less usual thing, due in all cases
perhaps, as it evidently is in 0. versicolor, to some unusual cause, such as the
stimulus caused by Asphondylia. There are many other species also in
which, as was noted by Griffiths (1913), the abnormal conditions of growth
provided in cultivation frequently induce persistence of the fruits.
Thirdly, the proliferation of the areoles of the ovary to flowers, while
apparently a nonnal occurrence in 0. arhuscula, 0. catacantha, and the
closely related 0. spinosissima, as it also is in 0. fulgida and Peireskia, is
a rarer phenomenon in the other four species mentioned, and in them occurs,
usually, if not always, under abnormal conditions.
Finally, the proliferation of the areoles of fallen fruits to roots and shoots,
thus to form new plants, may apparently occur in any of the seven opuntias,
but not in the soft, quickly ripening fruits of Peireshia.
THE FRUIT OF OFUNTIA FULGIDA. 51
Taking into account all four of the peculiarities mentioned, it is clear that
Opimtia fulgida is, on the whole, the most generally peculiar type studied,
followed most closely perhaps by 0. arhuscula and 0. catacantha. At the
other end of the graded series is Opuntia versicolor, which behaves like a
normal angiosperm in most, or perhaps all, cases where it is not stimulated
by the cactus fly, Aspliondylia.
It is evident (from observations made in Arizona, in the cactus garden
of the Bureau of Plant Industry established by Doctor Griffiths at Chico,
and from records in the literature, of cases such as Opuntia prolifera,
0. cJiolla, 0. spinodor, etc.) that many other species of Opuntia fit in at
various points in the series described above. In other words, in the genus
Opuntia the ovary, in flower and in fruit, may assume now more, now fewer
of the various functions of the vegetative joint. Of the Opuntia fruits thus
far studied from this point of view, that of Opuntia fulgida seems not only
the most atypical angiospemious fruit among these Cactacea?, but is perhaps
also the most aberrant (shoot-like) fruit to be found in all angiosperms.
PROLIFERATION OF JOINTS AND FRUITS IN
RELATION TO THE STERILITY OF FRUITS.
From what has been said above of Opuntia fulgida it is evident that the
propagation of this cactus has ceased to depend chiefly on the development of
fertile seeds, and so of seedlings, but is accomplished more largely by the
vegetatix-e sprouting of fallen joints and of fallen fruits. The propagation
of the species by the rooting of joints or parts of joints is rather common in
several genera of Cactacea?, such as Cereus, Mammillaria (Goebel, 1889),
Peircslda, etc., in addition to many and probably most species of Opuntia.
The propagation by means of the fallen fniit is probably common among
opuntias with persistent fruits. Besides its occurrence in the forms already
mentioned, it is apparently common also in 0. prolifera, 0. cholla, 0.
spinosior, etc.
In a number of other opuntias and certain other genera there are devel-
oped, in addition to the true fruits and ordinary vegetative joints, more
specialized short joints which are often bead-like or more or less fruit-like in
character. These occur, for example, in 0. arhuscula, 0. catacantha,
0. fulgida, 0. leptocaulis, 0. tetracantha (Toimiey, 1905), Mammillaria
gracilis (Goebel, 1889), a species of Cereus, etc. In each case these struc-
tures are capable, after falling, of taking root in the soil and tlius starting
new plants.
Taking this whole series of structures, together with the various sorts of
joint fruits that occur in 0. fuJgida and many other opuntias, and the many
seedless opuntia fruits, it might be assumed that the fruit of these Cactacefe,
and especially of the opuntias, is losing its primary function of seed-produc-
tion. ^ It is evident at least that the production of new plantlets and the
function of dissemination has been taken over in large part by these various
52 THE FRUIT OF OPUNTIA FULGIDA.
vegetative propagating bodies. This raises the question whether the seed-
bearing fruit of all opuntias is on the way to extinction, through a progres-
sive loss of the seed-bearing function, which may be expected to end in the
evolution of a totally sterile fruit, having no propagative functions other
than those that can be equally performed by vegetative joints.
It is true that the vegetative joints and both the fertile and sterile fruits
resemble each other greatly in their capacity for proliferation. There seems
no adequate reason, however, for assuming that either the proliferating habit
or the fundamental structure of the fruit is a secondary thing in the evolution
of the opuntias (Toumey, 1895). On the contrary, it is natural that the
thick-skinned, water-stored joints of these cacti should prove capable of per-
sisting on moderately moist soil until rooted deeply enough to secure a water-
supply adequate for the starting of a young plant. The fruit being, as we
have seen, really a stem in organization, up to the latest phase of its develop-
ment, it is also very naturally capable of proliferatiou to root and shoot.
The capacity of joint and fruit for persistence and proliferation is probably
as old as the fleshy character of the family. The persistence of the sterile
fruits, at least to maturity, is not a really surprising thing, in view of the
preponderatingly vegetative and stem-like character of the bulk of the wall
of the ovary. Sterile ovaries occur in many species of angiosperms, but in
most of these the carpels constitute the bulk of the fruit. Therefore, when
the seeds are wanting in these forms, and the carpels as usual fail to develop,
no fruit is formed and the flower bud soon withers and drops off. In
Opuntia, on the contrary, even if the seeds and carpellary portion of the
fruit do fail to develop, the basal stem-like part may go on, practically
unhindered in its vegetative growth, and mature quite normally.
When these facts concerning the comparative structure and behavior of the
stem and ovary of Opuntia are considered, in conjunction with the fact that
leaves are present on both and with the undoubted similarity of Opuntia to
Peireskia, there seems no adequate reason for believing that the fniit of
Opuntia is, structurally, an advanced type among the Cactacese. On the
contrary, Opuntia and its close relative Peireskia (which also has a leafy
ovary, the areoles of which, in the flower, proliferate to secondary flowers)
probably show us the simplest type of the inferior (submerged) ovary char-
acteristic of the Cactaceae. The capacity of the Opuntia fruit for persistence
and proliferation is to be regarded as the natural outcome of its original
morphological composition — i. e., a joint with an ovary immersed in its apex.
It seems clearly not a result of a marked degeneration of a once less stem-
like and more constantly fertile fruit, such as has been assumed ])y some
investigators to have been present during the evolution of the genus. The
more specialized or highly evolved flowers and fruits, structurally, among the
Cactacese are probably to be sought in such genera as Cereus, Rhipsalis, and
Mammillaria.
THE FEUIT OF OPUNTIA FULGIDA. 53
SUMMARY AND CONCLUSIONS.
The fruits of certain opuntias differ from those of other angiosperms,
except those of some Australian " bottle-bnish " trees, in not ripening and
then either opening or falling from the plant when the seeds are mature.
On the contrary, the peculiar fruits of these Cactacese and MyrtacesG remain
attached to the plant and actively growing for several or many years.
The persistent fruit of Opuntia fulgida is still more abnormal in another
respect, for it not only remains attached, unripened and steadily growing,
season after season, but the seeds are never shed from the fruit. Further-
more, the matured fruit itself, or even the ovary of the unopened flower,
while still attached to the tree, may give rise to secondary flowers and so to
other fruits. Four or five generations of flowers and fruits may thus be
formed in a single season. Finally, if a mature fruit falls on moist soil it
may develop adventitious roots and shoots and thus initiate a new plant.
This tree-like opuntia has a tuberculate and spiny cylindrical stem and
branches, the fleshy joints of which on separation readily sprout to new
plants.
The early development of the ovary of the flower in Opuntia fulgida
closely resembles that of a young vegetative joint, and the structure resulting
from this early development, with its minute, evanescent leaves, its tubercles,
and axillary areoles, is entirely stem-like in appearance. Only with the
initiation of the perianth, stamens, and carpels does the fertile joint become
distinctly flower-like in character. The ovarian cavity finally becomes com-
pletely buried in the stem-like, basal portion of the ovary, by the more rapid
growth of this portion upward and inward about the base of the carpels.
The whole outer wall of the ovary and fruit is thus a stem in its morpho-
logical origin. This is clearly indicated not only by the more general fea-
tures of development noted, but also by the identity in details of development
and structure of the tubercles and areoles, and of the photosynthetic and
water-storing tissues in the stem and fruit. In its physiological capacity
for persistence and for proliferation to flowers and shoots, the wall of the
fruit shows again its essential identity with the stem. Finally, the graded
series of structures intermediate in character between joint and fruit, sen-e
to further emphasize the likeness of the two.
The development of the flower of this opuntia indicates that it has evolved
from one with an originally superior ovary through the progressive submer-
gence of this ovary by the more vigorous growth of parts of the fertile joint
that were laid down before the carpels themselves were even initiated. Tliis
is probably a relatively primitive type of flower among the Cactacese, from
which the type found in Cereus and Echinocactus has been derived.
The perianth, the stamens, and the style are cut off from the top of the
ovary, a day or two after the flower withers, by the formation of a highly
developed, cup-shaped abscission layer. Any cells of the fruit except those
54 THE FRUIT OF OPUNTIA FULGIDA.
of the vascular bundle may participate in the formation of the cells of the
abscission layer. The cells of the vascular bundle in line with the abscission
layer seem to degenerate and rupture as a result of the split in the adjoining
tissues. The whole funnel-like scar left at the top of the ovary by the fall of
the perianth is soon protected by several layers of periderm. These arise
from a phellogen formed but a few layers within the abscission layer. One,
or sometimes several, layers of this periderm may have the cell-walls greatly
thickened to form a schlerenchymatous protective layer.
From the axillary buds, or areoles, of the primary flowers that open in
May, arise secondary flowers which open in June. From areoles of these, in
turn, tertiary flowers open in July, and on the latter quaternary flowers
bloom forth in August. Thus four and sometimes five generations of flowers
may be formed each season. Often two or three and sometimes four genera-
tions of persistent fruits may thus arise in a single summer.
The number of well-matured seeds occurring in a fruit may range from 0
to 100 or even 200. Large numbers of sterile seed-rudiments of various
sizes are found in most fruits, some of them evidently having degenerated
soon after their initiation. The fertile seed contains a large coiled embryo
and a small mass of endosperm in the loop between radicle and cotyledons.
The seeds of this opuntia have not, so far as is recorded, been Icnown to ger-
minate in the field under natural conditions. They were germinated in the
laboratory by slightly chipping the seed-coat. The seeds may remain
unchanged and capable of germination for several or many years while
embedded in the pulp of the persistent, attached fruits, or even in that of
fallen, rooted ones. The seeds are set free in nature only by the decay of
the pulp of the fallen fruit, or when the fruits are eaten by browsing animals.
It is possible that the failure of the seeds to germinate in the moist pulp of
the fruit, even during the hot summer, may be due to the impenetrability of
the seed-coat. Even chipped seeds, however, do not germinate in this
medium as they do in soil or on wet filter-paper, which suggests that the pulp
may have an inhibitory effect on some process connected with germination.
The mature fruit, unripened, remains attached to the tree after the ripen-
ing of the seeds. It may thus persist and grow year after year, by the aid
of a cambium ring. It is this persistent fruit that gives rise to flowers, just
as a stem would. By the proliferation of the primary flowers, so formed,
secondary and tertiary flowers arise and develop to persistent fruits, two,
three, or even four generations per season. In the course of several years a
cluster may arise containing scores of fruits with sometimes 10, 12, or even
14 generations of fruits in a continuous linear series.
Only in two cases, among hundreds examined, were attached fruits found
proliferating to vegetative joints.
Fallen fruits that rest on moist ground may give rise to adventitious roots,
from areoles, perianth-scar, or stalk-scar, and then to vegetative shoots, from
areoles only, and thus initiate new individual plants. In nature this origin
THE FRUIT OF OPUNTIA FULGIDA. 55
of new plants from fallen fruits is the most important means, next to prolif-
eration of fallen joints, of the multiplication and dispersal of this cactus.
The difference between the product of an areole of an attached fruit and
one of a fallen fruit that has rooted seems probably due to a difference in the
kind of nutritive (organ-building) material brought to the two areoles under
these different conditions. It is possible that the presence of roots on the
fallen fruit inhibits the formation of flowers by it.
Persistence and proliferation of the fruit, though not elsewhere as fre-
quent as in Opuntm fulgida, is not unknoA\Ti in other species. In Opuntia
versicolor, as also in several flat-jointed opuntias, the frequent persistence of
the fruit or even of the unopened flower is the result of the puncture of the
flower-bud by the cactus fly, which lays its eggs in it. In other cases, like 0.
catacantha, the factors that inhibit ripening and induce persistence are as
undetermined as they are in the case of 0. fulgida.
The fact that Opuntia fulgida and other species have series of fruits show-
ing various degrees of sterility, from those with scores of seeds to those that
are entirely seedless, can not be taken as conclusive evidence that seed-produc-
tion is really on the way to complete extinction in these plants. ISTeither is
the corollary that propagation by seeds is being replaced by the proliferation
to new plants of fallen fruits as significant as it might at first seem. On the
contrary, the stem-like character of the fruits in this genus results in the per-
sistence of many sterile ovaries, such as would, in many less fleshy angio-
sperms, wither and fall off soon after blooming, instead of maturing into
seedless fruits, as they do here.
56 THE FRUIT OF OPUNTIA FULGIDA.
LITERATURE CITED.
Caspaei, H. 1883. Beitrage der Kenntniss des Hautgewebes der Cacteen. Zeit.
fur Naturwiss., 2, pp. 30-80.
Cbockeb, W. 1906. Role of Seed-coats in Delayed Germination. Bot. Gaz., 42, pp.
265-290.
Daebishire, O. V. 1904. Observations on Mammillaria elongata. Ann. of Bot., 18,
pp. 375-416.
Debet, M. H. 1846. Proliferation d. Fruchtknotens lieferte eine Opuntia Salm-
Dyckiana. Verhandl. d. Naturhist. Ver. Preuss. Rheinl., 3, 83, 84.
Delavaud, M. C. 1858. Inflorescence du Peireshia bleo. Bull. Soc. Bot. de France,
5, p. 685.
Delbbouck, C. 1875. Die Pfianzenstacheln. Hanstein Botan., Abhandl. 2, pp. 1-119.
Engelmann, W. 1887. " Cactacese of the Boundary," in Botanical Works. Edited
by W. Trelease and Asa Gray. Cambridge, p. 212.
EwAET, A. J. 1907. The Delayed Dehiscence of CalUstemon rigida. Ann. of Bot, 21,
pp. 125-137.
Ganong, W. F. 1894. Beitrage zur Kenntniss der Morphologie und Biologic der
Cacteen. Flora, Erganzungsb., pp. 49-86.
. 1898. The Comparative Morphology of the Embryos and Seedlings of the
Cactace*. Ann. of Bot., 12, pp. 423-474.
GOEBEL, Karl. 1886. Zur Entwickelungsgeschichte des Unterstandigen Frucht-
knotens. Bot. Zeit, 44, pp. 729-738.
. 1889. Pflanzenbiologischeschilderungen. I. Kakteen, pp. 67-108.
Griffiths, D. 1913. Behavior, Under Cultural Conditions, of Species of Cacti
Known as Opuntia. Bull. No. 31, U. S. Depart, of Agricult.
Harris, J. A. 1905. The Fruit of Opuntia. Bull. Torrey Bot. Club, 32, pp. 531-536.
HiLDEBRANDT, F. 1888. Ueber Bildung von Laubsprossen aus Bliithensprossen bei
Opuntia. Ber. d. deutsch. bot. Gesellsch. 6, pp. 109-112.
Kauffmann, N. 1859. Zur Entwickelungs. d. Cactaceenstacheln. Bull. Soc. Imp.
des Naturalistes de Moscow, 32, part II, pp. 585-603.
Lauteebach, C. "W. 1889. Untersuchungen iiber Bau und Entwickelungs der Sekret-
behalter bei des Cacteen. Bot. Centrbl., 37, p. 257.
Lloyd, F. E. 1907. Observations on the Flowering Period of Certain Cacti. Plant
World, 10, pp. 31-39.
. 1916. Abscission in MiraUlis jalapa. Bot Gaz., 61, pp. 213-230.
Meehan, T. 1888. Opuntia Fruits. Gard. Chron., 3, p. 328.
Noll, F. C. 1872. Zwei Abnormitaten an Cactusfruchten. Ber. d. Senckenbg.
Gesell., 1872, p. 118.
Penzig, 0. 1890. Pflanzenteratologie. Genoa.
Schleiden, M. J. 1845. Beitrage zur Anatomie des Cacteen. Mem. I'Acad. Imp. d.
Sci. d. St Petersb., ser. 6, vol. 4, pp. 335-380.
Schumann, K. 1894. " Cactacese." Engler u. Prantl, III, Qa, pp. 156-205.
. 1890. Flora Brasiliensis, IV, 2.
SoLEREDER, H. 1908. Systematic Anatomy of the Dicotyledons. Engl. Transl., pp.
406-415.
TouMEY, J. W. 1895. Vegetal Dissemination in Opuntia. Bot. Gaz., 20, pp. 356-361.
— . 1898. The Tree Opuntias of the United States. Bot. Gaz., 25, pp. 119-124.
. 1905. Notes on the Fruits of Some Species of Opuntia. Bull. Torr. Bot.
Club, 32, pp. 235-239.
Wettebwald, X. 1889. Blatt- und Sprossbildung bei Euphorbien und Cacteen.
Nova Acta Kaiserl. Leopold. Carol., Ak. 53, pp. 379-440.
Wolfe, F. A. 1912. Notes of the Anatomy of Opuntia lindheimeri. Plant World,
15, pp. 294-298.
ZuccABiNi, J. G. 1836. Plantarum novarum vel minus cognitarum, etc. Fasc.
tertius, Cactacese. Abhandl. Muench. Akad., Math, physik. Klasse, 2,
pp. 599-742.
THE FRUIT OF OPUNTIA FULGIDA. 57
EXPLANATION OF PLATES.
ABBREVIATIONS USED IN PLATES.
a., areole or cushion formed by axillary bud; a. I., abscission layer; &., bristle or
glochidium ; bb., barb of bristle or of spine; c, carpel; ck., cork; cm., cambium;
c. c, crystal containing cell; c. t., conducting tissue of style; c. to., cell-wall; c, epi-
dermis; em., embryo; ep., endosperm; /., flower; fu., funiculus or stalk of ovule;
g. c, guard-cell; g. p., growing-point; h., hypodermis; i., integument; I., leaf; l. s., leaf-
scar; n., nectary; o., ovary; ov., ovule; p., petal; ph., phellogen; pi., palisade; p. s.,
perianth-scar; r., root; s., sepal; sa., stamen; s. c, slime-cell; sd., seed; sg., stigma;
sh., sheath of spine; so., stoma; sp., spine; st., stem; sy., style; t., trichome; tb.,
tubercle; v. b., vascular bundle; w. f. wall of fruit.
Frontispiece.
Photograph of a mature plant of Opuntia fulgida on reservation of Desert Laboratory
at Tucson, showing a frequent type of forked trunk, due to injury of main
axis, also the branching habit and clusters of fruit. The nesting bird is the
cactus wren, Heleodytes brunneicapillus couesi (Sharpe). [D. T. MacDougal
photo.]
Plate 1. Photographs of Opuntia fulgida.
Fig. 1. A fruiting plant growing in the desert at Tucson. Photographed April 25,
1915. X 0.03.
Fig. 2. Heavily fruiting branches of a tree on the campus of the University of Arizona.
The largest cluster included more than 100 fruits. Photographed in
May 1912. X 0.1.
Fig. 3. A single large cluster of fruits from the same tree as figure 2. X 0.3.
Fig. 4. A vegetative joint and fruits of 1914 bearing buds of flowers of 1915. Photo-
graphed in May 1915. X 0.6.
Plate 2. Photographs of 0. fulgida.
Fig. 5. Tip of a vegetative joint with young joints still bearing the evanescent leaves,
showing also areoles with spines and nectaries. X 0.9.
Fig. 6. Four generations of flowers and fruits developed from a vegetative joint in the
season of 1915. This cluster, collected at Tucson and photographed in
mid-July 1915, shows the relative sizes of the four generations. No. I
opened in May; II in June; III, if not removed from the plant, would
have opened in late July; IV in late August. Note that some members
of generation III (at right below) have but barely pushed out of the
areole. X 0.6.
Fig. 7 a, b, c. Joint-fruits and pseudo-fruits, showing several structures combining in
various degrees the characters of vegetative joint and fruit. X 0.45.
Fig. 8. Cluster of 11 secondary fruits borne on a single primary fruit showing the
persistence of fruits over one, two, or more winters. Photographed
April 1915. X 1.
Fig. 9a. Joint of 1914 bearing opened and withered flower of 1915, the latter with
buds of secondary flowers on its sides. X 0.6.
FiQ. 9&. Similar joint bearing primary flowers. In the areoles of these are borne
trichomes, nectaries, and buds of secondary flowers. Many of the latter
bear numbers of the awl-shaped deciduous leaves. X 0.6.
Plate 3. Drawings of O. fulgida.
Fig. 10. Radial section of an axillary bud of flower, showing growing-point, nectary,
spine, etc. X 25.
Fig. 11. Longitudinal section of a flower bud through a placenta, mammillae, leaves,
two axillary buds, a nectary, etc. X 3.33.
58 THE FRUIT OF OPUNTIA FULGIDA.
Fig. 12. Enlarged drawing of the areola shown at left in figure 11. It would probably
have developed a flower if it had been left on the plant. X 25.
Fig. 1.3. Part of a longitudinal and radial section of an unopened flower, bearing the
very young bud of a secondary flower at right. X 5.
Fig. 14. Longitudinal section of a young flower bud arising from the edge of the
perianth-scar on the fruit of the preceding season, showing leaves, very
prominent tubercles, and growing-points of the areoles on the adaxial
faces of the latter; showing also the shriveled nectaries developed in the
preceding season. X 12.
Fig. 15. Longitudinal section of a slightly older flower than that shown in figure 14,
showing the depression of the growing-point and the initiation of the
stamens. X 18.
Fig. 16. Longitudinal section of a still more advanced flower, showing the much
sunken growing-point and three series of stamens on each side of it.
X 18.
Fig. 17. Longitudinal section of flower with all stamens and carpels initiated. The
two upper areoles now face upward instead of axially. X 9.
Fig. 18. Part of a longitudinal section of a young flower showing further closing in of
the carpels above the cavity of ovary to form stylar canal. X 24.
Fig. 19. Longitudinal section of upper part of a slightly older flower, showing style
with free tips that are to form stigmas. X 17.
Fig. 20. A section, similar to that in figure 19, of a flower in which the placentae are
just distinguishable; at base of nectary at left is a leaf-scar, and below
the nectary is the vascular bundle that led to leaf. X 8.
Fig. 21. Longitudinal section of a half-matured flower, showing ovules just initiated,
stamens differentiated to anther and filament, etc. X 5.
Fig. 22. Longitudinal section of a flower nearly ready to open, showing ovules, style
with its conducting tissue, the papillose stigmas, and tightly over-
lapped sepals and petals. X 4.5.
Plate 4. Drawings of 0. fulgida.
Fig. 23. Longitudinal section of a flower that has just commenced to open, showing
ovules, papillose recurved stigma-lobes, etc. X 4.
Fig. 24. Longitudinal section of a young fruit from which the perianth and stamens
have recently fallen, showing the funnel-shaped scar with its corky
lining layer. X 3.
Fig. 25. Longitudinal section of a primary fruit with ripe seeds bearing a secondary
fruit, showing relative size of fruits and degree of development of seeds,
the connection of vascular systems, etc. X 1.5.
Fig. 26. Longitudinal section of two matured fruits, one or two years old, with
aborted seeds of various sizes, though fruits are plump and normal in
external form. X 1.25.
Fig. 27. Longitudinal section of a mature fruit, showing the usual shape of fruit, its
perianth-scar, areoles, and vascular system, also ripe seeds, together with
other seeds that have withered at various stages of development. X 1.25.
Fig. 28. Longitudinal section of a combination joint fruit, one or two years old,
showing the relatively small portion of its length occupied by the
ovarian cavity, which in this case contained only half-matured withered
seeds; showing also the vascular system and the prominent tubercles,
the one at the right with two spines. X 1.5.
Fig. 29. Transverse section of young flower bud showing petals, sepals, leaves, and at
left one spine. X 10.
Fig. 30. Transverse section of same bud lower down, showing the six stigmas, petals,
sepals, leaves, and the very prominent tubercles with their areoles;
showing nectaries, spicules, etc. X 5.
Fig. 31. Transverse section of the bud shown in figure 29, at level of the styles and
stamens. X 5.
Fig. 32. Transverse section of the bud shown in figure 29, at level of the ovarian
cavity, showing first rudiments of ovules. X 5.
THE FRUIT OF OPUNTIA FULGIDA. 59
Fig. 33. Transverse section of the sterile base of the same flower bud as that shown
in figure 29, showing the ring of vascular bundles, with fascicular
cambium already established. X 5.
Fig. 34. Transverse section of an older flower bud through seven styles or stigmas,
the stamens, petals, and sepals. X 5.
Fig. 35. Part of an approximately transverse section of the flower shown in figure 34,
giving details of structure of style and stigma, including the papillose
lining of the stylar canal. X 20.
Plate 5.
Fig. 36. Part of transverse section of a stigma, showing papillose surface, and the
conducting tissue, vascular bundle, slime-cells, etc., within. X 75.
Fig. 37. Transverse section through the flower shown in figure 34, showing style,
stamens, and wall of ovary with its tubercles, areoles, etc. X 3.
Fig. 38. Part of transverse section of young ovary, showing long-stalked ovules with
integuments initiated, and archesporial cell differentiated. X 24.
Fig. 39. Transverse section of a young ovary, showing seven placentas with numerous
anatropous ovules, also the vascular structure and radial arrangement
of photosynthetic cells in tubercle. X 4.
Fig. 40. Transverse section of slightly older ovary, showing the filling up of the
ovarian cavity by the growth of the young ovules and their stalks. Note
that the magnification is but half that of figure 39. X 2.
Fig. 41. Transverse section of mature ovary showing two nearly ripe seeds and a
larger number of sterile seeds that have ceased growing at various
stages of development. X 2.
Fig. 42. Transverse section of a persistent, fertile fruit several years old, showing
seeds and their stalks completely filling ovarian cavity, the great radial
growth of the vascular bundles, and the loss of prominence of the
tubercles. X 2.
Fig. 43. Transverse section of the sterile base of a fruit like that of figure 42, show-
ing the large central mass of water-filled parenchyma, the radial growth
of the vascular bundles from the activity of the fascicular cambium, and
the generally smooth, rounded outline of the surface. X 2.
Fig. 44. Transverse sections of vascular bundles from ovaries of various ages, all at
same magnification, to show relative growth of the phloem and xylem
regions of the bundle, (a) From ovary of a flower from which the
perianth has just fallen; (ft) from one-year fruit; (c) from a fruit 6 or
8 years old, 35 millimeters in diameter. X 11.
Fig. 45. Transverse section of lower third of nearly mature leaf from the ovary of a
flower about ready to open, showing flattened form, vascular system,
slime-cells, and the slightly specialized palisade. X 42.
Fig. 46. Transverse sections near tip of leaf from flower bud, showing small vascular
strand, slightly developed palisade, and large air-canals. X 50.
Fig. 47. Surface view of a flower bud some time before opening, showing sepals and
petals and six areoles. Two of the latter have already initiated flower
buds, in which the spindle-shaped leaves of lower part of ovary and the
flattened sepals and petals can be distinguished. Each of the remaining
areoles shows a leaf-scar and the dense tuft of trichomes, with its inner
border of spicules and its one or several embedded nectaries. X 3.
Plate 6.
Fig. 48. Part of transverse section near top of opening flower, showing upper surface
of an areole and a cross-section of the subtending leaf. Among the
trichomes of the areole are ten nectaries, and about its inner border is a
group of a dozen or more bristles or glochidia. X 2.
Fig. 49. Part of a transverse section of a recently opened primary flower, showing
edge of cup of flower and three tubercles, one of them bearing an areole
with two nectaries and the bud of a secondary flower. The arrow indi-
cates the sagittal plane. X 3.
60 THE FRUIT OF OPUNTIA FULGIDA.
Fig. 50. Radial or sagittal section of an areole of a primary flower, showing the
growing-point or stem apex of the areole, its bordering groups of bristles
and trichomes, two nectaries, and the subtending leaf. X 18.
Fig. 51. Three typical trichomes from an areole, showing their swollen tops and
slender bases. X 45.
Fig. 52. A single trichome from an areole, showing thick-walled pitted cells of tip.
X 110.
Fig. 53. A mature spine, showing the swelling at base, the barbed tip, and the trans-
parent sheath attached for its lower sixth, while the upper five-sixths of
it is loose and has slipped down by splitting and folding near the base
to leave the tip of the spine exposed. X 5.
Fig. 54. The upper fourth of an immature spine, showing in detail the intact striated
sheath and the barbed tip of the spine itself. X 50.
Fig. 55. Transverse section of a spine from a young fruit, showing the sheath of
loosely packed hairs and the spine with its core of closely compacted
small cells and its outer layers of large thick-walled barb-cells. X 110.
Fig. 56. Part of a sagittal section of an areole, showing a nectary with bristles and
trichomes at its base, with the separated, cutinized layer of the epi-
dermal cells at its tip; also the vascular supply of the nectary and of
the subtending leaf. The leaf is just being cut off to leave a relatively
small leaf-scar. X 45.
Fig. 57. Surface view of upper half of a mature spicule or glochidium, showing the
barbs closely resembling those of spines. X 72.
Fig. 58. Longitudinal section of basal fourth of a nearly mature bristle, showing
internal structure, barbs, and zone of rupture at which bristle breaks
off. X 125.
Fig. 59. Transverse section near middle of an immature spicule, showing the large,
thickened surface cells which are to give rise to the barbs. X 225.
Fig. 60. Longitudinal section of upper half of opening flower, showing the most fre-
quent location of the abscission layer, which cuts off the whole perianth
from ovary, but leaves style to be cut off independently. X 3.
Fig. 61. Section similar to that in figure 60, showing another type of abscission layer,
which cuts off the style as well as the perianth. Separation has already
occurred in the left half, while the abscission cells on the right are in
the stage shown in figure 67. X 3.
Fig. 62. Part of longitudinal section of wall of an ovary from which the perianth has
fallen, showing surface left after the break through the youngest cells
of the abscission layer. The arrow is parallel to the basal part of the
style. (Cf. figure 67.) X 48.
Fig. 63. Part of radial section of perianth-scar of very young fruit, showing phellogen
layer and cork. Abscission surface at right. X 117.
Fig. 64. Part of radial section of perianth scar of a two-year old fruit, showing the
parenchyma of fruit at left, phellogen in the middle, and cork at right.
X 110.
Fig. 65. Small portion of section similar to that in figure 64, showing structure of two
of the thickened cells in the cork. X 225.
Fig. 66. Outline of vascular system of inner petal. X 5.
Plate 7.
Fig. 67. Part of the radial section of ovary of newly opened flower illustrated in
figure 59, showing various stages in the division of cells that are forming
the abscission layer. The arrow is parallel to the style. X 110.
Fig. 68. Part of radial section through ovary of an opening flower, showing the rela-
tion of the abscission layer to the vascular bundles and to the mucilage
cells. X 19.
Fig. 69. Part of transverse section of two-year vegetative joint, taken through a
tubercle just below its areole, showing the structure of the epidermal
and of the palisade-like chlorophyll-containing tissues of the stem.
X45.
THE FRUIT OF OPUNTTA FULGIDA. 61
Fig. 70. Transverse section of a two-year vegetative joint, at about 2 centimeters
above base, showing vascular bundles and the radiate arrangement of
the palisade tissues in each tubercle. (Cf. figures 39 and 43.) X 1.5.
Fig. 71. Part of transverse section of tubercle of an unopened flower, showing epi-
dermis, stomata and palisade with its intercellular air spaces. X 205.
Fig. 72. Small portion of transverse section of two or three year old fruit, showing
details of stomata of the epidermis and its thick-walled underlying
layers. X 365.
Fig. 73. Small portion of transverse section of tubercle of similar fruit, showing
resemblance of the palisade, etc., to that of the vegetative joint. (Cf.
figure 69.) X 110.
Fig. 74. Part of tangential section of tubercle of a two-year vegetative joint, showing
palisade cells and mucilage cells in cross-section. X 85.
Fig. 75. Section of one of the crystal-holding cells so abundant in the subepidermal
and parenchymatous tissues. X 365.
Plate 8. Photographs 76 to 79, 0. fulgida; 80, Caixistemon; 81, O. ^-ersicolob.
Fig. 76. Lateral view of a five months' seedling, showing hypocotyl, cotyledons, and
first joint of stem. Seed planted April 27, 1917; photograph of living
seedling made October 12 following. X 0.9.
Fig. 77. Part of a cluster of fruits collected at Tucson in April 1915, showing one
chain of 14 links in a single linear series. X 0.3.
Fig. 78. Plantlet 10 months old, developed in a greenhouse in Baltimore from a fallen
fruit, showing position of adventitious roots and structure of the new
shoots. X 0.66.
Fig. 79. One of the two examples found in which the persistent fruits of 0. fulgida,
while still attached, proliferate to vegetative branches. Collected and
photographed at Tucson in April 1915. X 0.45.
Fig. 80. Branch of Callistemon speciosum, with three generations of flowers and
fruits, showing the persistence and growth of the firm green capsules.
Flowers at the tip about to open. Collected on the campus of the Uni-
versity of California in March 1916. X 0.23.
Fig. 81. Gall fruit of 0. versicolor. Collected and photographed at Tucson in April
1915, showing the curling of the abortive petals and the fly Asphondylia,
which has just escaped from one of the pupa cases projecting from the
side of the gall below the fly. X 0.3.
Plate 9. Photographs of 0. versicolor.
Fig. 82. A branch of 0. versicolor bearing several clusters of fruits and galls of 1914,
and groups of flower buds of 1915. Some of fruit-like structures are
clearly galls, but others are nearly, if not quite, normal. Collected and
photographed at Tucson, May 1915. X 0.45.
Fig. 83. A piece of a vegetative joint of 0. versicolor collected at Tucson in April
1915, showing 3 types of persistent fruits or galls. X 0.6.
Fig. 84. Four types of gall fruits of 0. versicolor, showing, at left, a slightly devel-
oped perianth; and, at right, a very liighly developed perianth. Col-
lected and photographed at Tucson in April 1915. X 0.45.
Fig. 85. Branch of 0. versicolor with two galls of 1913 or 1914. One of these bearing
two vegetative branches developed in 1914, and each of these a cluster of
flower buds for 1915. Collected and photographed at Tucson in May
1915. X 0.45.
Fig. 86. Branch of O. versicolor, showing persistent fruit (normal?) bearing a vege-
tative branch which is directed backward toward base of the parent
branch. Tucson, April 1915. X 0.45.
62 THE FRUIT OF OPUNTIA FULGIDA.
Plate 10. Photographs of O. discata, 0. cylixdrica, O. leptocaclis, and
o. catacantha.
Fig. 87. Portion of joint of O. discata bearing a gall fruit with projecting pupa cases
from which the cactus flies have just escaped. X 0.45.
Fig. 88. Tip of a joint-fruit of 0. cylindrica of 1913, bearing a persistent fruit of 1914,
two flowers and a vegetative joint of 1915. Note constriction only,
instead of the usual distinct articulation at base of the parent fruits.
X 0.45.
Fig. 89, a, b, c. Three branches of 0. leptocaulis bearing fertile fruits of 1914, sterile
fruits, various forms of more or less fruit-like branches, and also (c)
flower buds for 1915. X 0.45.
Fig. 90. A single joint of O. catacantha bearing four chains of fruits (all sterile),
showing one chain of six links on right and a single open flower on left.
Collected at St. Thomas, Virgin Islands, May 1915. X 0.45.
Fig. 91. Series of fruits of 0. catacantha (from same collection as those in figure 90)
in surface view, also in longitudinal and transverse section, showing
perianth-scar and small sterile ovarian cavity. X 0.45.
Plate 11. Photographs of Peireskia, Opuntia rxjfida, 0. arbuscula, and
O. leptocaulis.
Fig. 92. Two generations of flowers of Peireskia guamacho, showing proliferation
of primary flower from axillary buds at the level of the ovarian cavity
(indicated by an x). The primary flower and the secondary one at
right are shown in median longitudinal section. X 0.6.
Fig. 93. Flower and fruit of Peireskia guamacho, showing umbilicate fleshy fruit
with areole on right side above. X 0.9.
Fig. 94. A joint of 0. rufida bearing three persistent fruits, from one of which a new
vegetative joint has arisen. X 0.45.
Fig. 95. Two lower branches of 0. arbuscula bearing persistent fruits, and these, as
well as the normal vegetative joints, bearing slender condensed shoots
with closely packed areoles. X 0.45.
Fig. 96. Branch of 0. leptocaulis showing fruits and fruit-like branches, like those
described for figure 89. X 0.45.
Plate 12. Drawings of O. fulgida.
Fig. 97. Tangential section of half-grown seed, perpendicular to the flattened sides of
seed and passing through micropyle, showing pocket of funiculus which
incloses the seed and the two integuments. X 95.
Fig. 98. Section of ripe seed in plant of greatest diameter, showing embryo, endo-
sperm, integuments, and thick wall of funicular pouch with its included
vascular bundle. X 17.
Fig. 99. Longitudinal section of a fruit which has given rise to a new plantlet, show-
ing the portion of the fruit cut off by a layer of cork from participation
in the new plant. X 1.33.
Fig. 100. Longitudinal section of a fallen fruit through the point of origin of an
adventitious root from the border of an areole. X 14.
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