CHAPTER I

INTRODUCTION

1. What are galls?

Most of us are familiar with plant galls or cecidia. Some galls, like
the familiar oak-apple or the gall-nut produced by cynipids on
Quercus LINN. (fig. tAl, have been well known in medicine and
industry since time immemorial. Others like the bedeguar on Rosa
LINN. (fig. IE), the lenticular gall on leaf (fig. 84A), the gouty gall on
stem and the roly-poly galls produced by cynipids on different spe-
cies of Querc~ts LINN., the kammergalls of Pontania COSTA on Salix
LINN. (fig. tD), the spirally-twisted covering gall on the petiole of
Populus pyramidalis LINN. (fig. IC) and the gladstone-bag-like pouch
gall on Pistacia LINN. (fig. IB) produced by aphids, the large woody
galls on the branches of Acacia spp. produced by the fungus
Uromycladium (Plate I, 5) or the spherical, solid, pellet-like galls on
leaves of diverse plants (Plate VII), to mention only a few, though
perhaps not so well known, are not, however, less common and are

Fig. 1. Some common plant galls. A. The common oak-apple gall of Diplolepis
quercus-folii (Linn.) on Quercus pedunculata Ehrh. B. The gladstone-bag-like gall of
the aphid Aploneura lentisci Pass. on the leaflet of Pistacia lentiscus Linn. C. The
spirally twisted covering gall of Pemphigus spirothecae Pass. on the petiole of Popu-
lus pyramidalis Linn. D. The kammergall of Pontania on leaf of Salix. E. The
well known "bedeguar" gall of Diplolepis (=Rhodites) rosae (Linn.) on leaf of Rosa sp.

even more interesting for their complexity of structure, develop-

ment and ecological relations.
Galls are pathologically developed cells, tissues or organs of

M. S. Mani, Ecology of Plant Galls

© Springer Science+Business Media Dordrecht 1964
2
plants that have risen mostly by hypertrophy (over-growth) and
hyperplasy (cell proliferation) under the influence of parasitic or-
ganisms like bacteria, fungi, nematodes, mites or insects. They
represent the growth reaction of plants to the attack of the parasite
and are in some way related to the feeding activity and nutritional
physiology of the parasite (635, 639). Some galls, like, for example, the
so-called procecidia, are, however, known to arise even before the
parasite starts feeding (fig. 2A-B). COSENS 221 , 222 therefore consi-
dered as galls "any enlargement of plant cell, tissue or organ, indu-
ced by the stimulus of a parasitic organism as a regular incident in
the life of the parasite."

Fig. 2. Procecidia. A. Section through the kammergall of Pontania capreae Linn.

on Salix triandra Linn. showing the initiation of cecidogenesis even before the
hatching of the larva from the egg. B. L.S. through the kammergall of Pontania
viminalis Linn. on Salix purpurea Linn. (Modified from Beijerinck).

In the biological association between the gall-inducing parasite or

the gall-maker and the plant, it is the gall-maker that apparently
derives all the benefit and the plant suffers loss of substance, devia-
tions in the direction of growth, disturbances in sap flow, premature
decay, increase of non-essential parts at the cost of essential and
other injury. By producing the gall, the plant seems to have not
only guaranteed free shelter but also free nourishment to the gall-
maker and even to assure the dispersal of the species of gall-maker.
Even when there is some benefit to the gall-bearing plant, as for
example, in the fixation of atmospheric nitrogen in the root-nodule
gall produced by Bacterium radicicola (BEYER.) on Leguminosae
(fig. 28B) or in the cross pollination of flowers by the gall-forming
fig-insects (Blastophaga GRAVENH.) in Ficus spp., it seems to be
rather indirect and incidental. Although nearly all early definitions
of gall have laid considerable stress on this teleological aspect, it has
nevertheless been suspected that galls may be passive means of
defence on the part of the plant against the parasite. COOK 214 be-
lieved, for example, that the formation of a gall is "probably an
effort on the part of the plant to protect itself from an injury which
is not sufficient to cause death." ZWEIGELT1296~1299 has recently
developed the idea that the formation of a gall is the result of a
gradual process of mutual adaptation between the gall-inducing
 3

organism and the gall-bearing plant. The plant produces the gall
primarily not for the benefit of the gall-inducing organism, as
formerly assumed. The primary reaction of the plant to the gall-
inducing organism is not in the interest of the organism, but repre-
sents a sort of "struggle against the attack of the parasite," the
object of which is the neutralization of the toxins produced by it.
In so far as the reaction of the plant favours the survival of the or-
gan attacked by the gall-inducing organism, the primary advantage
in the formation of the gall is to the plant. By producing the gall, the
.planLhas in a sense loc;;alized the parasite in space and time and has
lorced it to extreme_specialization. Considered from this point of
yiew, a gall includes all structural deformities produced by plants
under the influence of a foreign organism, which may either be a
parasite or. a symbiote.
Particular attention must be drawn to the fact that the abnormal
structures which constitute galls are actively produced by the plant
as a result of abnormal growth activity. Galls are essentiallydevel-
opmental and growth abnormalities. This peculiarity will therefore
at once exclude a variety of abnormal structures, which are actively
produced by diverse animals on plants, but are not the result of
abnormal growth reaction on the part of the plant. The cigar-
shaped or barrel-shaped leaf scrolls made by different species of
weevils like Attelabus LINN., Rhynchites HERBST., etc., the rolling
and webbing of the leaf blade by caterpillars of certain moths like
Gracilaria, spiders, etc., for example do not represent the growth
reaction of the plant to the attack of these species and are therefore
not galls. In these cases the role of the plant is a purely passive one. We
must also similarly exclude from our concept of gall the well known
acarodomatia sometimes found on leaves, especially at the meeting
point of some of the principal veins, as hairy outgrowths, in which
mites like T arsonemus live. These hairy outgrowths are normal
features in the leaf structure, which are merely taken advantage of
by the mites and do not likewise represent the growth reaction of
the plant to the attack of the mite. A pathological structure, to be
considered as gall, must thus represent the reaction of the plant in a
specific manner, viz. by growth, to the attack of some foreign species.
The gall is essentially the product of an interspecific association
between a plant and another organism, characterized by the plant
reacting with growth, which is abnormal in some respect.
While there is usually very little difficulty in recognizing a gall
as such, one often comes across cases, which are, however, not so
readily classed. The difficulty is partly due to the fact that we usually
find every gradation between the apparently normal and the deci-
dedly abnormal growths, so that it is often extremely difficult to be
sure whether a given deformity is worthy of being called a gall.
There is also no hard and fast rule to decide at what stage of abnor-
4

mality a growth becomes a gall. Some workers include, for example,

the mere curling of a developing leaf blade under the influence of
thrips, aphids, etc. under the term gall, but others do not consider
such deformities as galls, unless the curling is at the same time also
accompanied by more or less pronounced swelling of the part. As
growth is associated with cell hypertrophy, cell proliferation or both,
wherever these processes are observed to arise under the influence
of foreign organisms, we deal with galls. The fundamental character
of a gall, as distinct from numerous other abnormal structures we
find commonly on plants, is that the reaction of the plant to the
attack of a foreign organism includes, without exception, these
processes.
Even among the decidedly abnormal growths, one often comes
across instances which are galls according to some workers, but not
according to others. The mines in leaves produced by the larvae of
certain insects illustrate some of the difficulty, we often find in
determining galls. Leaf mines, in which the mesophyll surrounding
the mine does not produce any new formation or growth, has no
significance to our concept of gall. In these cases the plant remains
more or less passive. In most cases, there is thus little doubt, but
in the case of mines produced by certain species there is sometimes
considerable cell proliferation, so that the mined leaf is also more
or less conspicuously swollen, in addition to being passively crumpled
and otherwise deformed. The active callus outgrowths from the
uninjured neighbouring cells develop into the mined cavity gener-
ally as a tube-like or bladder-like thin-walled, plasma deficient but
hyperhydric mass and may contain some chlorophyll or may lack
this pigment altogether. The mined cavity seems in this case to
particularly favour the growth of callus regenerative tissue. In the
simplest case, the callus growth consists of typical, large branched
cells. This is found, for example, in the leaf mines of Pegomyia
chenopodii ROND. on Chenopodium album LINN. and Chenopodium
urbicum LINN. and Rhynchaewus quercus LINN. on Quercus. The new
tissue formed in these cases develops conspicuously near a vascular
element and at some distance behind the mining larvae and is
apparently not directly related to the feeding activity of the larvae.
Abundant callus outgrowth fills the mine of Phytomyza ilicis
CURT. in the leaf of !lex aquifolium LINN. The larva feeds as a rule
on the uppermost of the multi-layered palisade and the lowermost
layer now exhibits cell proliferation and callus outgrowth in the
form of a multi-layered, elongate tubular mass, so that even the
epidermis becomes locally pushed upward to form a conspicuous
bulge on the surface of the leaf blade. Such mines have a remarkable
resemblance to what is usually known as parenchyma or pustule
gall (vide Chapter VII). The epidermis is, for example, very con-
spicuously bulged outward in the mine of Liriomyza strigata MEIG.
 5
In all these mines the neoplastic tissue is apparently the result of
stimulus of mechanical injury and there is probably no direct
specific relation to the mining larva. In the mines of other species,
the larva at first mines in the midrib. From this main gallery the
larva then produces some lateral galleries and often sometimes
returns to the main gallery at a later stage to feed on the new regener-
ative tissue which has filled the gallery in the meanwhile. This
callus regenerative tissue thus corresponds to the so-called nutritive
tissue found in many typical galls (fig. 41). The larvae of the Micro-
lepidoptera N ePtic~tla argyropeza ZETT. andN epticulaturbidellaZETT.
mine in the distal part of the petiole. The mined portion becomes
swollen to about twice the normal thickness. Initially the mining
larva is found in a gallery in parenchyma, with hypertrophied cells.
VOIGT 1221 considers the mines of Apion sedi GERM. on leaf of Sedum
spp. as galls on the basis of their histological peculiarities. Examples
of leaf mines associated with such cell growth and renewed cell
divisions and filling up of the lumen of mine with new tissue should
be included among galls.
It should be pointed out that not all growth abnormalities arise
at the seat of attack by the gall-maker, but sometimes involve distant
organs also. The effect of the attack of the gall-maker does not
seem to be strictly localized in such cases or perhaps the develop-
ment of a gall in a distant part may be the secondary result of some
as yet unrecognized effect at the seat of attack. In such cases the
deformities do not generally show evidence of the presence of a
parasite inside them. The inflorescence of many plants, for instance,
may undergo anomalous development due to the attack of gall
Nematodes and certain insects inside the root underground, far from
the actual place of deformity. The gall midge Rhopalomyia hypogaea
F. Low develops in the stem of Chrysanthemum leucanthemum in
many parts of Europe and causes the non-development of the ray-
florets in the capitulum. MOLLIARD B10 has described several such
growth abnormalities in flowers of Scabiosa columbiaria LINN. due
to the attack of H eterodera marioni (CORNU) Goo DEY within the
root. Such growth abnormalities also constitute galls.
A number of galls are therefore essentially abnormally developed
organs and are known as "organoid galls". The typical organoid
galls include fasciations produced by mites, fungi and other orga-
nisms (fig. 3), abnormally elongated or abnormally stunted inter-
nodes and bunched leaves, abnormally shaped leaves, doubled and
filled-up flowers, chloranthy (virescence) or greening of the petals
of flowers, petalloidy, witches' brooms, etc. The abnormality is thus
largely or also exclusively in the external form of the part, but the
anatomical and histological structures do not differ fundamentally
from those of the normal plant organ. The tissues of organoid galls
are thus normal. Some of the organoid galls are often extensive
6

growths and involve the major part or the whole of the aerial por-
tionof a plant (Plate II. 3). Organoid galls are predomin antly produced
by parasitic fungi (especially the Uredinaceae, Ustilaginaceae,

Fig. 3. Fasciation of the shoot axis of Hibiscus canabinus Linn.

Exoascaceae, etc.), mites and aphids and only exceptionally by

Diptera and Hymenoptera. They develop also on all classes of plants.
Most galls are, on the other hand, far more complex in their
structure and we cannot recognize in them any normal organ as such.
These galls differ fundamentally in their anatomy and histology
from the normal organ on which they arise and in contra-distinc-
tion to organoid galls, they are termed histioid galls.

2. The fundamental character of a gall

The essential character of a gall, however, is not really its cause
- what gives rise to it - and its relation to the causative factor or
even its structure, but its relation to the plant on which it arises -
to the morphogenetic control of the plant body. A gall is essentially
a neoplastic growth. Neoplastic growths are pathological structures,
ranging from the nearly normal to the highly complex and abnormal
outgrowths, characterized by cellular hypertrophy and hyperplasy.
The cell growth and cell divisions in the gall are not coordinated with
these processes in the normal organ. Abnormal cellular hypertrophy
and hyperplasy are induced in plants as in animals, by diverse
factors (vide Chapter XIV). Irrespective of the causative factor
 7
and complexity of the structure of a gall, there is in its development
a more or less pronounced departure from the general morphogenetic
restraint of the organ of the plant. Depending upon the degree of
this departure, galls may be limited neoplasms or unlimited neo-
plasms. Neoplasms are described as "spontaneous" if internally
conditioned and "induced" if externally conditioned. Most naturally
occurring neoplasms on animals are usually presumed to be internally
conditioned 321 , but some animal neoplasia like the virus tumors,
viz. the Shope papilloma1044, Brown-Pearce tumor of rabbits 148 ,
Rous sarcoma of fow1985-987, the Bittner mammary tumor of mice 88
and the cysticercus tumor of rat3 25 are considered as "induced".
Tumors induced by the action of various carcinogens are externally
conditioned. The line of demarcation between the so-called inter-
nally conditioned and the externally conditioned ileoplastic growths
is not, however, sharp and at any rate the distinction is purely ar-
bitrary. The Shope papilloma, for example, ordinarily benign,
becomes malignant as a result of the combination with agents, which
are themselves only mildly carcinogenic in action 988 . Most of the
tumors now classified as spontaneous will doubtless eventually be
found to be induced on fuller investigation. Spontaneous neoplasms,
so called, are generally rare on plants and .are restricted, as at pre-
sent known, to the relatively mild and delimited chimeras, fascia-
tions, etc., due to somatic chromosomal mutations or hybrid in-
compatabilities as in the case of the genetic tumors on crosses of
Nicotiana glauca with Nicotiana langsdorji (vide Chapter XIV).
In limited neoplasms, the morphogenetic character of the galled
tissue does not depart widely from that of the normal plant. The
abnormal growth does not proceed beyond the strict limits in space
and time set by the specific nature of the plant. Chimeras, fascia-
tions; galls by mites, nematodes and insects (zoocecidia) (vide
Chapter IX); galls by fungi (mycocecidia, vide Chapter XII), etc., are
some of the better known examples of limited neoplasms on plants.
Limited neoplasms may be non-biological or biologicalinorigin. The
non-biological limited neoplasms are galls induced by physical and
chemical means.
The physical galls include the callus outgrowth at the margins of
wounds. While mechanical injury is naturally the initial cause, a
combination of derangements of water economy and respiratory
rates, accumulations of the products of necrosis, all of which are
essentially chemical changes, represents the immediate cause of the
wound regeneration callus outgrowths. VOCHTING1217 showed that
over-growth at the point of union of stock and scion in a graft
results from the tendency of the individual cells of both the stock
and scion to maintain their definitive polarities. Physiologically like
cells of both animals and plants (vide Chapter XIV) exhibit repul-
sion, so that their distal ends tend to avoid the distal ends of adja-
8
cent cells and to approach the proximal ends. As the plant cells are
not, however, capable of free movements to correct such unsuitable
polarity orientations, such a correction can only come about by
growth (fig. 149). Each new cell, as it is being formed, tends to be
orientated to bring about adjustments between stock and scion.
The result is an intumescence. The term intumescence was first
applied by SORAUER to localized, pustule-like swellings of tissues
due to the enlargement of cells on Ribes, Eucalyptus rostrata
SCHLECHT., Acacia pendula A. CUNN., Lavatera trimestris, Aloe
grand~fiora, A phelandra porteana, etc. The cortical cells often become
radially elongated, especially on the sunny side, thus giving rise to
loose swellings. These swellings become considerably large where the
cells of the primary cortex are involved. Intumescences are also
widely known on leaves and localized knob-like swellings arise either

Fig. 4. T.S. through intumescence on leaf of Cassia tomen/osa (Modified from Sorauer).

on the upper or also on the under side of the leaf blade in the form
of green or white pustules of variable height and diameter. Some of
these hypertrophied cells may also undergo division. ThIS is, for
instance, met with in the well known intumescence on leaf of Ficus
elastica LINN., Ruellia formosa and Cassia tomentosa (fig. 4). The
epidermis above the intumescent mesophyll becomes either simply
bulged out as in Epilobium hirsutum or may also become in its turn
hypertrophied, highly modified, with abnormally shaped stomata.
Although the galls referred to above are initiated by purely
physical causes, it is, however, incorrect to assume that their devel-
opment is not subsequently influenced by chemical factors. There
is indeed no sharp dividing line between the so-called physical and
chemical galls and in most cases both the initial and proximal
causes are predominantly only chemical (vide Chapter XIV). It is
known, for example, that even ordinary salt water and solutions of
copper salts produce intumescence on leaves and stems1036 . Organic
acids like malic acid, acetic acid, formic acid, butyric acid, lactic
acid, etc., are well known for their tumefacient effects on diverse
plants 35, 97. In 1932, DOLK & THIMANN274 demonstrated the
 9

growth-promoting activity of indole-acetic acid. Formic acid has

also been shown to be of some importance in the formation of certain
insect galls. The wour.d hormones, considered to stimulate the for-
mation of regeneration tissue 426 , also appear to involve certain
acid products. The heterauxins like indole-acetic acid, indole-
butyric acid, naphthalene-acetic acid, etc., have well known tume-
facient properties and may perhaps be in part least responsible for
the formation of a many of our insect galls 146 , 347, 629, 630. Most of
the chemical-induced intumescences are, with few exceptions, limi-
ted neoplasms and develop only so long as the external force of the
chemical is available in the plant tissues.
Limited neoplastic galls of biological origin include the virus galls,
bacterial galls, fungal galls, mite and insect galls, nematode galls,
etc. Some viruses produce definite tissue distortions and the enations
induced by certain strains of the tobacco mosaic virus are examples
of this type (90-92, 549;) (vide Chapter XIII). BLAcK 90 has described
a definitive virus tumor on a wide and varied range of plants. The
gall-making virus is a systemic entity, but the gall arises only where
local tissue proliferation is initiated by injury. Thus neither injury
nor the virus alone seems to be capable of producing the gall, but
when the cells invaded by the virus are injured, they are incited
to rapid and disorganized growth and division. Though superficially
non-limited in character, it is of course difficult to determine how
the cells of the gall would behave in the absence of a chronic infec-
tion by the virus. Bacterial galls occur on a great variety of plants
and some of them, like the root nodule galls of Leguminosae, are
typically limited neoplastic galls (vide Chapter XIII). Fungal galls
are too varied and numerous to be mentioned at this stage (vide
Chapter XII) and there is at present no evidence that any mycoce-
cidia ever become autonomous and non-limited. The zoocecidia are
typically limited neoplastic galls. We must not, however, overlook
the possibility that the limited character of the growth of these
galls may actually be the result of nutritional or structural barriers,
rather than intracellular physiological barriers, as may be generally
assumed.
The galls, which we have so far considered, arise as a result ofthe
presence of a foreign body of some kind and continue to develop only
so long as this body or its immediate chemical products are present
within the plant tissue and are thus in this sense strictly exogenous.
In EWING'S terminology 321 these limited neoplastic galls are
"irritation teratoma". Although numerous attempts have been made
to establish the similarity of plant galls to malignant growths on
animals and man, it has been pointed out that vegetable neoplastic
growths are mostly traceable to some recognizable and persistent
stimuli, but the animal neoplasia are of unknown origin (vide
Chapter XV). The discovery of virus and chemical tumors of ani-
10

mals has, however, weakened this objection. Certain galls are truly
autonomous, at least in their final stages of development and are
therefore typical non-limited neoplasms. In non-limited neoplasms
the degree of abnormal growth is not controlled by the nature of the
plant but only by the exciting factor. In 1912, SMITH and his
collaborators l064 described the development of galls on Chrysan-
themum jrutescens, inoculated with the bacterium Phytomonas
tumejaciens (SM. & TOWNS.), as consisting of a tumor at the site of
inoculation and secondary tumors at distances, often three or four
internodes away from the site of inoculation. The secondary tumors
arise in leafaxils, on midribs, petioles and seldom on the stem proper
and are not connected with the primary tumor by continuous tumor
tissue. As the secondary tumor does not develop in the stem tissue im-
media tel y ad j acentto the primary tumor, itis notthe result of direct
diffusion of the bacterial metabolic products or even of the primary
tumor. Also the bacterial sterility of the secondary tumors does not
conform with the idea of "irritation teratoma". Though SMITH did
not recognize the importance of his own observations, recent re-
searches have demonstrated that the secondary tumors are truly auto-
nomous: their origin is independent of the causative factor, once the
initiation has been effected. JENSEN 548 demonstrated the trans-
plant ability of the secondary tumors. By grafting the bacteria-free
secondary tumor tissue onto Beta vulgaris of different colours (for
example, red tumor tissue grafted onto yellow healthy tissue and
vice versa), JENSEN showed that there is no deep tissue invasion
by the tumor tissue. The tumor corresponds to JENSEN'S rat sar-
coma or artificial metastasis of animal tumors. BRAUN & WHITE
later132 successfully cultivated the bacteria-free fragments of the
secondary tumor on in vitro media and established the characteristic
independence of the tumor tissue. The tumor character was further
proved by transplanting fragments of the tumor tissue cultures onto
healthy tissues. The cause of the pathological condition is in the
tumor cell itself and not in any accompanying organism. The tumor
cells are endowed with the qualities of disorganized growth and
division, both in vitro and in vivo and with the capacity for trans-
plant ability or artificial metastasis. The genetic tumors of Nicotiana
hybrids, already mentioned, are also non-limited neoplastic galls.
The cells of the non-limited neoplastic galls are generally assumed
to be "permanently transformed" in some specific manner, but as
has recently been pointed out by HOUGH 536 , many cells of the
so-called "cecidial galls", bacterial galls and virus galls also undergo
irreversible transformation.
The term gall thus embraces a much wider range of morphogene-
tic abnormalities in plants than has hitherto been understood. A
general synopsis of a morphogenetic classification of abnormal
growths in plants, recently suggested by BLOCH 93 , also favours this
 11

wider concept of galls. A fundamental difference thus exists be-

tween the earlier and the present concepts of galls. In our concept,
there is a new emphasis on the ecological and morphogenetic aspects,
as distinct from the earlier and rather narrowly morphological
approach. Our approach to the problems of galls thus centres around
the dynamic aspect rather than on the static structural. Whether we
consider the term gall in a restricted sense or in its wider meaning,
we must, however, recognize the fact that the concept is strictly
ecological. A gall is essentially the product of mutual interaction of
the plant cell and the gall-inducing agent. The development of a
gall involves factors that release a cell from the general morphogene-
tic coordinating influences. For a correct understanding of the com-
plex problems of gall formation, the inducing factors, the plant
reactions, etc., an ecological approach is therefore a fundamental
necessitv.