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Bulletin 332 February, 1939
UNIVERSITY OF FLORIDA
AGRICULTURAL EXPERIMENT STATION
GAINESVILLE, FLORIDA
WILMON NEWELL, Director
NAILHEAD SPOT OF TOMATO
Caused by Alternaria tomato (Cke.) N. Comb.
By GEORGE F. WEBER
i,.- ..
Fig. 1.-Old nailhead spots on a ripe tomato.
TECHNICAL BULLETIN
Bulletins will be sent free to Florida resident upon request to
AGRICULTURAL EXPERIMENT STATION
GAINESVILLE, FLORIDA
EXECUTIVE STAFF
John J. Tigert, M.A., LL.D., President of
the University
Wilmon Newell, D.Sc., Director
Harold Mowry, M.S.A., Asst. Dir., Research
V. V. Bowman, M.S.A., Asst. to the Director
J. Francis Cooper, M.S.A., Editor
Jefferson Thomas, Assistant Editor
Clyde Beale, A.B.J., Assistant Editor
Ida Keeling Cresap, Librarian
Ruby Newhall, Administrative Manager
K. H. Graham, Business Manager
Rachel McQuarrie, Accountant
MAIN STATION, GAINESVILLE
AGRONOMY
W. E. Stokes, M.S.., Agronomist'
W. A. Leukel, Ph.D., Agronomist
G. E. Ritchey, M.S., Associate2
Fred H. Hull, Ph.D., Associate
W. A. Carver, Ph.D., Associate
John P. Camp, M.S., Assistant
Roy E. Blaser, M.S., Assistant
ANIMAL HUSBANDRY
A. L. Shealy, D.V.M., Animal Husbandman'
R. B. Becker, Ph.D., Dairy Husbandman
L. M. Thurston, Ph.D., Dairy Technologist
W. M. Neal, Ph.D., Asso. in Dairy Nutrition
D. A. Sanders, D.V.M., Veterinarian
M. W. Emmel, D.V.M., Veterinarian
N. R. Mehrhof, M.Agr., Poultry Husbandman
0. W. Anderson, M.S., Asst. Poultry Husb.
W. G. Kirk, Ph.D., Asst. An. Husbandman
R. M. Crown, B.S.A., Asst. An. Husbandman
P. T.T Dix Arnold, M.S.A., Assistant Dairy
Husbandman
L. L. Rusoff, M.S., Asst. in An. Nutrition'
CHEMISTRY AND SOILS
R. V. Allison, Ph.D.. Chemist1
F. B. Smith. Ph.D., Soil Microbiologist
C. E. Bell, Ph.D., Associate Chemist
R. B. French, Ph.D., Associate
H. W. Winsor, B.S.A., Assistant
J. Russell Henderson, M.S.A., Assistant
L. W. Gaddum, Ph.D., Biochemist
L. H. Rogers, M.A., Spectroscopic Analyst'
Richard A. Carrigan, B.S., Asst. Chemist
ECONOMICS, AGRICULTURAL
C. V. Noble, Ph.D., Agricultural Economist'
Bruce McKinley, A.B., B.S.A., Associate
Zach Savage, M.S.A., Associate
A. H. Spurlock, M.S.A., Assistant
ECONOMICS, HOME
Ouida Davis Abbott, Ph.D., Specialist1
Ruth Overstreet, R.N., Assistant
ENTOMOLOGY
J. R. Watson, A.M., Entomologist'
A. N. Tissot, Ph.D., Associate
H. E. Bratley, M.S.A., Assistant
HORTICULTURE
G. H. Blackmon, M.S.A., Horticulturist'
A L. Stahl, Ph.D., Associate
F. S. Jamison, Ph.D., Truck Horticulturist
R. J. Wilmot, M.S.A., Spec. Fumigation Res.
R. D. Dickey, B.S.A., Assistant Horticulturist
J. Carlton Cain, B.S.A., Asst. Horticulturist
Victor F. Nettles, M.S.A., Asst. Hort.
PLANT PATHOLOGY
W. B. Tisdale, Ph.D., Plant Pathologist'
George F. Weber, Ph. D., Plant Pathologist
R. K. Voorhees, M.S., Assistarit3
Erdman West, M.S., Mycologist
Lillian E. Arnold, M.S., Assistant Botanist
BOARD OF CONTROL
R. P. Terry, Chairman, Miami
Thomas W. Bryant, Lakeland
W. M. Palmer, Ocala
H. P. Adair, Jacksonville
Chas. P. Helfenstein, Live Oak
J. T. Diamond, Secretary, Tallahassee
BRANCH STATIONS
NORTH FLORIDA STATION, QUINCY
L. O. Gratz, Ph.D., Plant Path. in Charge
R. R. Kincaid, Ph.D., Asso. Plant Pathologist
J. D. Warner, M.S., Agronomist
SJesse Reeves, Farm Superintendent
CITRUS STATION, LAKE ALFRED
A. F. Camp, Ph.D., Horticulturist in Charge
John H. Jefferies, Superintendent
Michael Peech, Ph.D., Soils Chemist
B. R. Fudge, Ph.D., Associate Chemist
W. L. Thompson, B.S., Asst. Entomologist
W. W. Lawless, B.S., Asst. Horticulturist
EVERGLADES STATION, BELLE GLADE
J. R. Neller, Ph.D., Biochemist in Charge
J. W. Wilson, Sc.D., Entomologist
F. D. Stevens, B.S., Sugarcane Agronomist
Thomas Bregger, Ph.D., Sugarcane
Physiologist
Jos. R. Beckenbach, Ph.D, Asso. Horticul.
Frederick Boyd, Ph.D., Asst. Agronomist
G. R. Townsend, Ph.D., Asso. Plant Path.
R. W. Kidder, B.S., Animal Husbandman
W. T. Forsee, Ph.D., Asst. Chemist
B. S. Clayton, B.S.C.E., Drainage Engineer'
SUB-TROPICAL STATION, HOMESTEAD
W. M. Fifield, M.S., Asst. Horticulturist
S. J. Lynch, B.S.A., Asst. Horticulturist
Geo. D. Ruehle, Ph.D., Asso. Plant Pathologist
W. CENTRAL FLA. STA., BROOKSVILLE
W. F. Ward, M.S., Asst. An. Husbandman
in Charge2
FIELD STATIONS
Leesburg
M. N. Walker, Ph.D., Plant Pathologist in
Charge
K. W. Loucks, M.S., Asst. Plant Pathologist
Plant City
A. N. Brooks, Ph.D., Plant Pathologist
R. N. Lobdell, M.S., Asst. Entomologist
Cocoa
A. S. Rhoads, Ph.D., Plant Pathologist
Hastings
A. H. Eddins, Ph.D., Plant Pathologist
Monticello
Samuel 0. Hill, B.S., Asst. Entomologist2
Bradenton
David G. Kelbert, Asst. Plant Pathologist
Sanford
R. W. Ruprecht, Ph.D., Chemist in Charge,
Celery Investigatitions
W. B. Shippy, Ph.D., Asso. Plant Pathologist
Lakeland
E. S. Ellison, Meteorologist2
B. H. Moore, A.B., Asst. Meteorologist'
'Head of Department.
'In cooperation with U.S.D.A.
30n leave.
CONTENTS
PAGE
INTRODUCTION ..........~................... ........... 5
THE DISEASE ......--- .......... .................... 5
Host range ..-----...- -- ..- ..---- -- .----........ ...... ....- ........ 5
Geographical distribution .. .. ------..... .....-......-.... ....-- 6
Economic importance .......... .. .. .... ...... .................... 7
Symptoms .........................----- ................. 9
CAUSAL ORGANISM ........... .....----... ---------...------..-- -- ....-............. 13
Taxonomy ...... ............. ......... ..... .... ...- -............... 13
Morphology ................ -- --- .......... --... ......--..--....---- 23
Physiology .......... ....................... .. ...---.....- ...--- .. 27
Germination of conidia ........--....-- ..--- .......------ ....-...------- -...... 30
Relation of temperature and light to growth of the fungus ........ 31
Growth of the fungus in relation to the reaction of the medium.... 31
Pathogenicity .............. ..........---- ....-... .. ........... 33
Isolation ... .......... -------. .-.. .-...............-. 33
Inoculation .... ................ ..... .. --- ...... ...... 34
FUNGUS AND HOST RELATIONS .........-...--. .-- .......3................... 39
Seasonal development of the disease ............... .......--- .....- .....---- 39
Longevity of the fungus ..-..........~-......-- -------..------.---.---. 40
7 Source of inoculum ..--............... ..---- ---..--....... --- ---- ..----........... 40
SSpore production -.................. ... ------------------ 41
Spore dissemination ............--......-............. ............ 43
Time and mode of natural infection .................... ........ ...... .... 44
Period of incubation and pathological anatomy ................................ 45
SUM M ARY ................................................ .......... ....................... 50
LITERATURE CITED .--- ........... ................--- --- .... ............. .............. 51
Fig. 2.-Tomato foliage infected by nailhead spot: Above, from young plants in the seedbed;
below, from bearing plants in the field.
NAILHEAD SPOT OF TOMATO
Caused by Alternaria tomato (Cke.) N. Comb.
By GEORGE F. WEBER
INTRODUCTION
Nailhead spot (caused by Alternaria tomato (Cke.) N. Comb.)
is an important disease of tomatoes in the Southeastern and
Gulf states, causing losses of plants and fruit in the field, and
of fruit in transit. The literature contains numerous articles
and references concerning this disease and the causal parasite,
but there is considerable confusion about the life history and
interrelationships of certain tomato leaf and fruit spots caused
by this and other closely related phytogenous fungi. During
the past 10 years, through continuous observations and investi-
gations, data have been accumulated in an effort to clear up the
situation. This paper presents a complete description of the
morphological and cultural characteristics of the parasite, its
host range, taxonomic position, means of identification of the
various phases of the disease which it causes on tomatoes, and
a complete review of the literature.
THE DISEASE
Numerous common names of this disease have been used by
tomato growers in various parts of the United States and in
Florida. Among those recorded by Burger (14)1, Rolfs (60)
and Sherbakoff (67, 68) are tomato rust, blight, leaf blight,
blackspot, scab, early blight, birdseye, black rot, French rust,
brown rust, nailhead, nailhead rust and nailhead spot, which
are more or less descriptive of certain phases of the disease.
Since the characteristic lesions on the fruit (Fig. 1) are the
most conspicuous and diagnostic stage of the disease, the term
nailheadd spot" is preferred as a common name by the writer
and will be used exclusively hereafter.
Host Range.-Nailhead spot has been reported to attack only
tomatoes under natural conditions, except for a single report
by Palmer & Westell (52) of it appearing on sweet peas in
England. There is considerable doubt as to the authenticity
of this identification. Under greenhouse conditions the host
range has been extended by means of artificial inoculation to
1Italic figures in parentheses refer to "Literature Cited" in the back
of this bulletin.
NAILHEAD SPOT OF TOMATO
Caused by Alternaria tomato (Cke.) N. Comb.
By GEORGE F. WEBER
INTRODUCTION
Nailhead spot (caused by Alternaria tomato (Cke.) N. Comb.)
is an important disease of tomatoes in the Southeastern and
Gulf states, causing losses of plants and fruit in the field, and
of fruit in transit. The literature contains numerous articles
and references concerning this disease and the causal parasite,
but there is considerable confusion about the life history and
interrelationships of certain tomato leaf and fruit spots caused
by this and other closely related phytogenous fungi. During
the past 10 years, through continuous observations and investi-
gations, data have been accumulated in an effort to clear up the
situation. This paper presents a complete description of the
morphological and cultural characteristics of the parasite, its
host range, taxonomic position, means of identification of the
various phases of the disease which it causes on tomatoes, and
a complete review of the literature.
THE DISEASE
Numerous common names of this disease have been used by
tomato growers in various parts of the United States and in
Florida. Among those recorded by Burger (14)1, Rolfs (60)
and Sherbakoff (67, 68) are tomato rust, blight, leaf blight,
blackspot, scab, early blight, birdseye, black rot, French rust,
brown rust, nailhead, nailhead rust and nailhead spot, which
are more or less descriptive of certain phases of the disease.
Since the characteristic lesions on the fruit (Fig. 1) are the
most conspicuous and diagnostic stage of the disease, the term
nailheadd spot" is preferred as a common name by the writer
and will be used exclusively hereafter.
Host Range.-Nailhead spot has been reported to attack only
tomatoes under natural conditions, except for a single report
by Palmer & Westell (52) of it appearing on sweet peas in
England. There is considerable doubt as to the authenticity
of this identification. Under greenhouse conditions the host
range has been extended by means of artificial inoculation to
1Italic figures in parentheses refer to "Literature Cited" in the back
of this bulletin.
Florida Agricultural Experiment Station
include eggplant, horse nettle and potato. Details of these tests
will be fully discussed under pathogenicity of the fungus.
Geographical Distribution.-The type collection of nailhead
spot of tomato was made in South Carolina. According to the
Plant Disease Reporter (77) and the Florida Agricultural Ex-
periment Station reports the disease has caused more or less
damage in the United States and Mexico for the past 25 years.
It was first reported in Florida in 1913 and continued to appear
annually thereafter. In 1919 it was found in all of the southern
Atlantic, Gulf and border states westward to California, and
continued within this range, including also Arkansas and Ten-
nessee, for more than a decade.
This gives an indication of the general range of the disease
in this country. However, there may be some question as to
whether these reports give the exact limits of the disease,
since in many instances the disease might not have been ob-
served or recorded unless it caused considerable damage. Dur-
ing the years 1931 to 1938 nailhead spot was noted in Florida
but was of little economic importance and consequently was
not included in the Reporter (77). The range of the disease
on the North American continent would probably include all
Central American countries where tomatoes have been grown
for a number of years, the West Indies, Mexico, and that portion
of the United States bordering on Mexico, the states in the lower
Mississippi basin and south of the Ohio River, eastward to the
Atlantic coast. Chupp (17) states that the disease is usually
not severe in the northern tier of states but may cause com-
plete losses in Indiana, New Jersey and southward. Weber and
Ramsey (82) report that it occurs in the entire tomato-growing
regions of Florida, while Pritchard (53) considered it very
prevalent all over the South. Stakman, Leach and Seal (69)
reported a blackrot of tomatoes in Minnesota which was distinct
from blossom-end rot but probably was not nailhead spot.
Baudys (4) records the disease in Czechoslovakia, Weber (80)
in Denmark, Britton-Jones (10) from certain Egyptian provinces,
and Erikson (32) from a number of countries of the old and
new worlds. There are certain additional reports of the disease
by Briosi (9) from Italy and Butler (16) from India who have
apparently confused it with blossom-end rot. At least, such
is the impression obtained from reading the reports. Cooke
(23) stated that tomato blackrot caused by the nailhead spot
parasite occurred in England, but his illustrations show the
Nailhead Spot of Tomato
blossom-end rot disease, indicating his apparent confusion of
the troubles. On the other hand, Bewley (6) stated that the
true nailhead spot is unknown in England.
Economic Importance.-Baudys (4) reported that there was
a severe outbreak of nailhead spot of tomatoes in Czechoslovakia
in 1930, whereas previously the disease had always been con-
sidered one of minor importance in that country. Butler (16)
commented on the destructiveness of the disease in India where
the chief damage resulted from fruit infection.
In the United States, Edgerton and Moreland (29) considered
losses from nailhead spot in Louisiana second only to those from
Fusarium wilt and stated that it was endangering the industry
in that state. They
cite, as an example
of its destructive-
ness, a 50 percent
loss in a 200-acre
field. Burger (14,
15) considered this
F'F. 3.-A deld of omna-
toe labosel heavily infected
~it-h nallhead apot and a
field of urnnleeed plant
right .
disease of tomatoes very important, stating that during certain
years practically all leaves on infected plants were destroyed
and the fruit was badly spotted, especially in the east coastal
region of south Florida. (Fig. 3.) Rosenbaum (63) stated
that ntilhead spot was by far the most destructive and wide-
spread disease of tomatoes with which the growers of south-
eastern United States had to contend.
Florida Agricultural Experiment Station
Nailhead spot has been the cause also of considerable loss
to shippers and brokers because of the destruction of packed
fruit in transit and in storage. Data accumulated by inspectors
of perishables at destinations have been presented by the Plant
Disease Survey (77), showing percentages of loss in car ship-
ments from various states. These data are extremely interest-
ing when consideration is given to field conditions in the various
states for the same seasons.
TABLE 1.-AVERAGE LOSSES OF TOMATOES FROM NAILHEAD SPOT IN CAR-
LOAD SHIPMENTS IN TRANSIT FOR THE FOUR-YEAR PERIOD, 1918-1921,
INCLUSIVE. ESTIMATED AT DESTINATION BY GOVERNMENT INSPECTION.
Year Origin No. of cars Percent loss
inspected at destination
1918 Florida 23 12
Florida 116 12-17
Texas 5 3-10
Arizona 1 5-8
1919 Georgia 1 15
Mexico 3 3
California 2 16
Louisiana 1 90
Mississippi 2 12
Florida 108 13
Arizona 1 6
1920 California 2 8
Mississippi 1 14
Texas 2 6
Mexico 5 7
Florida 38 1',
1921 California 1 1:i
Texas 1 11
West Indies 1 1C
The losses reported in Table 1 are peculiarly significant be-
cause the fruit concerned had been carefully graded for this
disease before it was packed. The amount of harvested fruit
that was rejected and sent to the cull pile has not been recorded
in many instances, although packinghouses have at times culled
out 40 to 50 percent of the fruit from the pickings oi' badly
infected fields. Again, fruit that was observed to bo badly
spotted by the pickers often was left in the field. Additional
reports by the Plant Disease Survey (77) show in Mississippi
Nailhead Spot of Tomato
a 3 percent loss in 1923 and 2 percent loss in 1925; in Alabama,
1 percent loss in 1925 and 1926, and 2 percent loss in 1927.
Losses in other adjacent states were comparable, while the total
loss in Mexico in 1927 was estimated to be $1,000,000.
Records show that nailhead spot was first recognized in Flor-
ida in 1913. During the following years there was a marked
increase in amount of losses up to and including 1925. These
losses were estimated as follows: 8 percent in 1916 and 15,
20, 30, 34, 30, 38, 50, 50, 40 percent, respectively, for succeed-
ing years. Since 1925 the disease has appeared each year but
at no time has it caused more than 2 to 4 percent loss. Reports
of only scattered occurrence were received during several sea-
sons, showing that it had almost disappeared from the state.
These percentages show an increase in importance of a rela-
tively unknown disease over a period of a few growing seasons,
to one of first importance and threatening a $10,000,000 in-
dustry. It had reached its zenith in destructiveness in 1923
and 1924, 10 years after its first recognition, causing millions
of dollars worth of damage, resulting in a loss of 50 percent of
the Florida crop for these two seasons. Beginning in 1925, and
continuing to the present time, it has become less important
until now it may be considered as unimportant as it was in 1914.
The reason for this marked reduction of the disease after
1925 may be partially accounted for by the almost universal
growing of the Marglobe variety. This variety was shown, by
the writer in 1924, to be resistant to the nailhead spot disease.
During 1925-26 and for several years thereafter this variety
was planted almost exclusively. However, during the last few
years other varieties have been planted in increasing acreages
and undoubtedly have been responsible for the annual occur-
rence of the disease.
Symptoms.-Partial or otherwise incomplete descriptions of
the symptoms of nailhead spot of tomato plants have been
published by Sherbakoff (67), (68), Taubenhaus (74), Cook
(21), Rosenbaum (63), McWhorter (45) and others. Nowhere,
however, does there exist, to the writer's knowledge, a syn-
drome of this disease. Certain descriptions apply only to seed-
lings; some apply to plants in the field and others include only
the fruit in the field, packinghouse or in transit. There also
exist numerous comparatively recent descriptions, Chupp (17),
Douglas (27), and Weber and Ramsey (82), which are not cor-
rect, but rather include symptoms of several tomato diseases that
Florida Agricultural Experiment Station
affect the stem, foliage or fruit, such as blossom-end rot, early
blight, bacterial spots, gray spot and Phoma rot. Consequently,
a complete description will follow, with special emphasis on the
distinguishing characters where confusion with other diseases
exists.
The earliest indication of nailhead spot may appear on the
foliage of seedlings (Fig. 2). Under these conditions the dis-
ease appears as small, circular or irregular, sunken, brownish-
black spots less than a millimeter in diameter. Individual spots
are usually evident from either surface of the leaf almost from
the time they become visible to the unaided eye. From their
initiation until they become several millimeters in diameter they
cannot be distinguished definitely from spots of Phoma rot, early
blight or gray spot of similar size and age, except by the fruit-
ing structures that may be present. As nailhead spots grow
older they tend to become more circular in outline with a slight
yellowing along the margin and the central blackish area often
fades to an avellaneous brown. Usually they do not become
more than half a centimeter in diameter except under extremely
humid conditions. The surfaces of the spots are smooth, but
occasionally dark concentric circular lines cause them to appear
rough and rugose. Spots located on principal veins become
elongate along the vbins of the leaf, and the blade area beyond
usually becomes prematurely yellow and dies. Often the in-
fections are numerous over limited areas and the spots coalesce
before becoming very large, rapidly killing the leaf. Heavily
infected leaves turn yellow and die very soon even though less
than 5 percent of the blade tissue is involved by the spots.
Conidiophores and conidia develop eventually on both surfaces
but usually they are more plentiful on the lower surface. Under
favorable conditions for their development they are so numerous
as to cause the spot to become fuscous and fumaginous in color.
The fungus continues to produce spores over the surface of the
infected leaves after they are dead and remain attached or
have fallen from the plant. Under ideal conditions of moisture
and temperature these leaves produce great numbers of spores
in a very short time. In contrast, similarly infected and dead
leaves that are not shed or which do not fall into favorable
surroundings produce very few additional conidia before they
disintegrate.
Stem infections may occur at any time during the life of the
plant. Stem lesions occurring on extremely young plants in
Nailhead Spot of Tomato
the seedling stage are most serious and the plants are usually
killed. The older the plants are at time of infection the less
the stem lesions affect the plant. Old, bearing plants often
show stem and branches almost completely covered with a
callous formed by coalescing infections. The resulting damage
is apparent, although measured with difficulty. Plants showing
this extreme diseased condition of the stem very seldom produce
uninfected fruit and leaves.
Infections on the stems are first evident by the appearance
of very small, barely discernible, dark green to brownish, more
-or less circular specks. As these lesions enlarge they become
sunken, darker colored and definitely circular. The older spots
that are 4 or 5 mm. in diameter often but not always show
light tan centers. Spots seldom exceed half a centimeter in
diameter except where widely spaced infections occur on a young
growing stem. Petioles, peduncles, and calyxes are subject to
infection.
Lesions on the fruit are the most conspicuous and diagnostic
symptom of the disease, as well as the most important eco-
nomically. Without fruit infection it is extremely difficult to
distinguish definitely, without microscopical examination of
spores, leaf spots of the nailhead disease from those caused
by any of several closely related parasites. Fruit infections,
however, remove all doubt as to the correct identification of the
parasite, since no other known fungus produces a comparable
lesion on tomato fruits. (Fig. 4.)
The earliest indications of fruit infection are the presence,
at any time during its development, of small, shallow, gray to
tan-colored specks anywhere on the surface. At this stage the
fungus has entered only the epidermal cells and the specks
appear to be almost superficial. On extremely young fruit
these spots enlarge and deepen rapidly, become grayish-black
and slightly sunken. When numerous they coalesce and often
cover almost the entire surface of the young fruit, calyx and
peduncle. Often the spots are clustered in smaller areas and
in such instances the developing fruit usually becomes irregular
in shape as it enlarges. When infection takes place on half-
grown fruit the spots are at first tan or brown. They may
develop as described above or they may remain quite shallow
and expand rapidly, producing a characteristic uneven border
surrounding a whitish area with a dark speck in the center,
where the infection probably was initiated. These light-colored
Florida Agricultural Experiment Station
spots gradually become sunken but less so than those originat-
ing on younger fruits. The color of the surface becomes darker
as the spots grow older because of the production of conidio-
phores and conidia. The fruiting structures first appear around
the dark, central speck followed by others in rapid succession
until almost the entire spot is covered. Spores are produced
abundantly also on the more sunken spots. The spots seldom
exceed a centimeter in diameter on the pear, plum and peach
(reference to shape) varieties; fruit spots average less than
Fig. 4.-Naturally produced nailhead spots in various stages of development on tomato
stems and fruit, compared with young infections caused by Bacterium vesicatorium Doidge,
lower right.
Nailhead Spot of Tomato
half a centimeter. On mature, colored fruit the spots are
characteristically rimose and sunken. Very often the host tissue
immediately surrounding the spot is green in contrast to the
pink or red color of ripe fruits. The spot itself has a narrow,
black border surrounding the whitish central area, which varies
in extent, depending on age of the spot and whether conidio-
phores and conidia are numerous. Older spots on ripening fruit
almost always penetrate to the seed cavity and if a spot occurs
over a locular partition the fungus penetrates to the core. After
the disease advances to this extent certain rapidly growing
secondary organisms often enter through the lesions and cause
gaseous putrescense. The symptoms here described are general
and inclusive for a large majority of specimens, although slight
variations may occur under some environmental conditions.
However, these characteristics as to type, rate of growth, and
size of lesion do not agree in details with the description pre-
sented by Nightingale and Ramsey (51).
CAUSAL ORGANISM
Taxonomy.-Nailhead spot was first collected and recorded
on ripe tomatoes in South Carolina by Ravenel, and the para-
sitic fungus was described and named by Cooke (22) in 1883
as Macrosporium tomato. These collections were designated as
No. 3099 and No. 603 in Ravenel's "New American Fungi"
deposited at Kew. (Fig. 5 top.)
The description was probably complete enough when it was
made but has caused considerable confusion among subsequent
workers. Galloway (35) apparently misinterpreted Cooke's
description of this parasite and the disease it caused when in
1888 he described a disease of tomatoes he considered to be
caused by Macrosporium tomato Cke., and labeled his illustra-
tion of it in Plate III, 1-7 as M. solani. This reference shows,
without doubt, (Fig. 5) the tomato disease known today as
blossom-end rot, a non-parasitic disease which affects the tissues
around the blossom end of tomato fruits. Galloway stated that
the fungus he found did not exactly conform with Cooke's
original description, but that bits of the fungus inserted under
the skin of ripe tomatoes caused decay. The writer has made
similar inoculations by inserting spores of the fungus Alternaria
fasciculata found on tomatoes affected with blossom-end rot
and has obtained a fruit decay. This decay, however, in no
way resembles nailhead spot. However, since Galloway's illus-
14 Florida Agricultural Experiment Station
by Macrosporium tomato Cke.. ;were the first published in the
(i- '.. '.
tesivy in more rent pliatis by Thaxter (), Mc
Carthy (44), Cobb (19), Stewart (72), Beach (5), Voorhees
(78), Earle (28), Tryon (76), Clinton (18), Halsted (37),
Quinn (54), Froggatt (34), Kirchner (42), Stone (73), Waters
by Macrosporium tomato Oke. were the first published in the
United States showing this trouble, they have been copied ex-
tensively in more recent publications by Thaxter (75), Mc-
Carthy (44), Cobb (19), Stewart (72), Beach (5), Voorhees
(78), Earle (28), Tryon (76), Clinton (18), Halsted (37),
Quinn (54), Froggatt (34), Kirchner (42), Stone (73), Waters
Nailhead Spot of Tomato
(79), Cotton (25) and Hosterman (38). Furthermore, Cooke
apparently overlooked his original description of the fungus
or at least the disease it caused since he (23) copied closely
Galloway's description and produced original colored illustra-
tions in his book showing blossom-end rot as the disease caused
by M. tomato Cke. Blossom-end rot, then thought to be caused
by a parasitic fungus, has been found by Brooks (11) to be of
physiological origin and certain secondary organisms usually
overgrow the exposed surfaces of the affected areas.
Alternaria and Macrosporium include both saprophytic and
parasitic species which are distinguished with difficulty even
by experts. However, the error of Galloway probably would
have been prevented if Cooke had included a few characteristics
of the disease with his original description of M. tomato.
To determine whether the fungus and disease causing so
much loss in Florida was the same as the type material of
Cooke, specimens of nailhead spot and blossom-end rot were
collected in Florida and sent to Kew for comparison with the
type material. Mr. Wiltshire made the comparison and re-
turned photographs of the type (Fig. 5 top) as verification
that the nailhead spot disease of tomatoes in Florida is caused
by M. tomato Cke. He wrote: "Ravenel's No. 603 resembles
the type collection No. 3099 completely. You will see they
(types) are very like your material of nailhead spot disease
in appearance and quite distinct from the blossom-end rot dis-
ease. Microscopically the fungus nailheadd spot) agrees with
the type of M. tomato very well and personally I think they
are the same species." The fungus and disease are entirely
comparable with the type. Blossom-end rot, as known by the
writer (Fig. 6) and described by Brooks (11), is an entirely
different disease and the Macrosporium sp. associated with it
is not M. tomato Cke.
A request, with accompanying photographs and specimens,
was sent to the New York Botanical Garden for comparison
with Ellis and Everhardts' collection of this fungus as listed
in their North American Fungi number 2848. Dr. Seaver made
the comparison and stated that the above Exsiccati was similar
to our nailhead spot. Consequently, their collection No. 2848
is authentic and comparable with the type. Gilman, in a letter
replying to the writer's request, stated that the report (36) of
M. tomato Cke. from Iowa was on a blossom-end rotted tomato,
which indicates that that reference to M. tomato Cke. was in-
Florida Agricultural Experiment Station
Fig. 6.-Tomato fruits affected with sunscald and blossom-end rot showing invasion of dead
tissue by the facultative parasite, Alternari fasciculata (C. & E.) J. & G.
Nailhead Spot of Tomato
correct. Darnell-Smith (26) reported blossom-end rot as bac-
terial in nature and that M. tomato Cke., the fungus often found
associated with this disease, was secondary. Jones and Grout
(41) placed M. tomato Cke. and Cooke & Ellis's (24) M. fas-
ciculatum, which they stated was a saprophytic fungus found
on many mature or dead plant parts, as synonyms of their
Alteraria fasciculata (C. & E.) J. & G. Cook (20) listed
M. tomato Cke. and A. solani (E. & M.) J. & G., a new com-
bination made by Jones & Grout from Ellis & Martin's M. solani,
as synonyms of A. fasciculata. Evidently he considered blossom-
end rot as caused by some different organism and A. fasciculata
as a secondary organism. Butler (16) stated that A. fasciculata
(C. & E.) J. & G. and A. solani (E. & M.) J. & G. occurred on
tomatoes and that although they were distinguishable both had
been referred to M. tomato Cke. He placed both M. tomato
and M. lycopersici Plowr. as synonyms of A. solani (E. & M.)
J. & G. which would imply that all three names refer to the
same parasitic fungus commonly found on tomatoes, causing
the disease known in Florida as early blight. This disease is
comparable with early blight of potatoes and distinct from
Septoria blight, which is often referred to as early blight of
tomato in the United States. In contrast, Kirchner (42) and
Jatzymina (40) have reported M. lycopersici as the cause of
blossom-end rot as illustrated by Galloway. This would lead
one to believe that M. lycopersici was saprophytic and synony-
mous with A. fasciculata (C. & E.) J. & G. instead of a com-
mon virulent parasite as referred to by Butler. Stevens (71)
and Seymour (66), apparently following the work of Jones
and Grout, have listed M. tomato Cke. as a synonym of A. fas-
ciculata (C. & E.) J. & G. Elliot (30) placed A. fasciculata
and M. tomato in the same group of saprophytic organisms in
his study of the species of these two genera because of the dif-
ficulty of distinguishing them without examination of pure
cultures or inoculation trials. Bolle (7) contended that A. fas-
ciculata and A. tenuis are identical, and Mason (47) believed
that A. tenuis was the species used by Nees as the type for the
genus Alternaria.
Freeman (33) asserted that the disease affecting fruit and
foliage which he called black rot was very similar to potato
early blight, and was caused by Macrosporium tomato Cke.,
and Massee (50) agreed that Ellis and Martin's (31) M. solani
was similar, if not identical with it. In an anonymous (2)
Florida Agricultural Experiment Station
note it was stated that a fungus often found on dying potato
leaves closely resembled M. solani E. & M., but was distinct
because it produced chains of 10 or 15 spores. It was further
stated that since M. tomato Cke. developed exactly similar chains
of spores in culture, the fungus found on potato leaves was
probably the same fungus, and since chains of spores were com-
mon to both, the fungus should be A. tomato Cke. (N. Comb.).
According to the writer's studies this statement of long chains
of spores cannot possibly refer to the nailhead spot parasite
because it is not known to produce spore chains of more than
three spores and very rarely any chains. Therefore, since this
anonymous author was not dealing with the nailhead organism,
and since the type material is definitely nailhead spot attributed
to M. tomato Cke., his binomial cannot stand.
Massee (48, 49, 50) illustrated black rot caused by M. tomato
Cke. and may have used authentic material for his illustrations,
since the lesions are not at the stylar end of the fruit. How-
ever, they are not at all characteristic of nailhead spot nor are
the illustrations of spores at all comparable with spores of the
nailhead-spot fungus. He stated further that cross and recipro-
cal inoculations where M. tomato and M. solani were used showed
these organisms to be identical. According to the writer's find-
ings the spores of these two fungi are distinguishable and the
diseases they cause on tomato foliage and fruit are very different.
Cooke (23) included an earlier edition of Massee's book (48)
as a reference but, as stated above, illustrated blossom-end rot
as the disease. Rolfs (60) reported nailhead spot to be caused
by A. solani (E. & M.) J. & G. and that it infected the leaves
of tomato plants. Sherbakoff (68) and Taubenhaus (74) listed
M. solani E. & M., a synonym of the previously mentioned fun-
gus, as the causal parasite. Edgerton and Moreland (29) and
Weber and Ramsey (82) designated A. solani (E. & M.) J. & G.
as the parasite causing nailhead spot. These last four references
are erroneous in that all referred to the nailhead spot disease
but none attributed it to M. tomato Cke., the true parasite.
Eriiksson (32), after studying the literature, stated that the
disease was described as being caused by A. solani in America
and M. tomato Cke. in England. Chupp (17), after reviewing
the literature, apparently was undecided and listed the disease
as caused by Macrosporium sp. Rands (59) did not include
M. tomato as a synonym of A. solani (E. & M.) J. & G. Douglas
(27) reported a fruit spotting caused by a species of Alternaria
Nailhead Spot of Tomato
that was different from A. solani and M. tomato. Rosenbaum
(61, 62) accepted the generally prevalent name M. solani (E.
& M.) for the nailhead spot disease; in fact, he intimated' that
early blight also was caused by this fungus. Later, however,
Rosenbaum (63) began to doubt that M. solani was the correct
name of the parasite and believed that M. tomato Cke. con-
formed more closely to the description of the fungus causing
nailhead spot and finally Rosenbaum and Sando (64) concluded
that nailhead spot was caused by M. tomato Cke. Samuel (65)
stated that M. solani E. & M. (a synonym of A. solani (E. & M.)
J. & G.) would not produce nailhead spots on tomatoes. The
writer has verified Samuel's statement frequently, but will add
that this fungus occasionally causes infections distinct from
nailhead spots at places other than at the calyx or stylar ends
of the fruits. Jakovleff (39) reported M. tomato Cke. as the
parasite causing a tomato disease in the Ukraine. Brinkman
(8) decided that M. tomato Cke. should be referred to the genus
Alternaria because he observed catenulate spore production by
the fungus in culture, which would validate such a transfer
and would result in the new combination A. tomato (Cke.)
Brinkman. The writer, at two different times, for a definite
check obtained from Dr. Johanna Westerdijk transfers of the
original fungous culture from which Brinkman obtained the cul-
ture with which he worked. Comparisons of Brinkman's culture
with the fungus isolated from nailhead spots on tomatoes in
Florida showed that the fungi were distinct and quite different.
The most striking difference between the cultures was the 8- to
15-spored chains produced by Brinkman's organism. In addi-
tion to the cultural characteristics, it was found through re-
peated inoculation experiments that Brinkman's fungus was
not pathogenic on tomato fruits, stems or leaves, whereas the
Florida isolant from nailhead spots used in parallel experiments
produced typical lesions on all parts of the tomato mentioned
above. The conclusion is that Brinkman was not working with
the nailhead spot organism and consequently the new combina-
tion of A. tomato (Cke.) Brinkman, which is based on the char-
acteristics of a fungus that is not pathogenic on tomatoes and
does not conform to the type material, cannot stand.
Further inquiry into the source of the Brinkman culture
showed that it was obtained from Dr. Westerdijk who in turn
had received it from Bailey. It was the same culture that had
been used by Ramsey and Bailey (55, 56, 57) and Nightingale
20 Florida Agricultural Experiment Station
and Ramsey (51) in their reported work. A culture of this
fungus was obtained from Bailey and a comparison of this with
the fungus with which Brinkman worked showed that the two
were identical. A further check on the organism was made by
sending a culture of the Florida fungus to Westerdijk for com-
parison with Bailey's culture, the source of Brinkman's culture.
The following reply was received: "In comparing your strain
of Alternaria tomato with the culture of 'Macrosporium tomato'
of Bailey, we found that they certainly are not identical." In-
oculation experiments were again conducted in which the fungus
received from Bailey was used parallel with the Florida isola-
tion. The results were similar to those previously reported
with Brinkman's culture; namely, that Bailey's culture was not
pathogenic. Because of this fact, and of the differences in num-
ber.of spores in chains and certain variations in cultural char-
acteristics, the writer has concluded that the fungus used by
Ramsey and Bailey (55, 56, 57) and Nightingale and Ramsey
(51) was not the parasite causing nailhead spot on tomatoes,
even though they referred to it as M. tomato Cke., and A. tomato
(Cke.) Brinkman.
The writer (81) suggested after considerable study, but with-
out knowledge of the work of Brinkman at that time, that the
---- --^-rH i-Wf-I--- /
=====----~^_ Jt
cZ /-----2?,
Fig. 7.-Camera lucida outline drawings of spores of the nailhead spot fungus produced in
culture, showing not more than two in a chain and irregularity of length of beaks.
Nailhead Spot of Tomato
name M. tomato Cke. should be changed to A. tomato (Cke.)
n. comb., because the fungus in culture occasionally produced
two-spored chains (Fig. 7). Comparisons and determinations
of the cultures as described above were made after Brinkman's
report was found.
Angell (1) stated that the production of spores in chains
should not be used as a basis for the separation of species of
the genera Alternaria and Macrosporium and that most of our
species in these genera should be placed in Macrosporium. Wilt-
shire (83) concluded that species of these two genera producing
spores with short beaks and in long chains and with long beaks
and in short chains should be included in Alternaria. The writer
agrees with Wiltshire's contention that practically all of the
present described species of Alternaria and Macrosporium
should be classified as Alternaria, which would include the fungi
with muriform conidia borne singly or in chains regardless of
whether they are beaked. This classification would be prefer-
able to that promulgated by Angell who would place all such
forms as mentioned above in the genus Macrosporium.
Studies of blossom-end rot, early blight and nailhead spot
and the associated organisms have shown that in Alternaria sp.
and Macrosporium sp. there is such a great variation in spore
size within a species that the exact measurements made by one
individual may vary considerably from those made by another.
The variation in size of spores of the same fungus in pure
culture and from the host or even between spores on different
hosts often is greater than the measurements between recorded
species. Spores in mass, however, from almost any species of
Alternaria show certain characteristics that will usually differ-
entiate them from the others. In this respect, without definite
spore measurements, M. tomato Cke., A. fasciculata (C. & E.)
J. & G. and A. solani (E. & M.) J. & G., the three closely related
fungi occurring on tomatoes, can be readily separated and
identified.
Cooke's (22) original description of the fungus is as follows:
Macrosporium tomato, Cooke in Ray. New Amer. Fungi. No. 603.
Orbiculare, atrum, Hyphis abbreviatis, robustis, flexuosi, sep-
tatis, Sporis clavatis, superne leniter attenuatis, deorsum vix
stipitatis, perenchymaticis fuscis (.1 .12 X .02 .022 mm.).
On ripe tomatoes (Ray. 3099) South Carolina.
It is known that the spores are obclavate rather than clavate
and that they are muriform-septate. Such corrections and the
22 Florida Agricultural Experiment Station
following additions should be made: "Spores borne singly or
rarely in chains of two or three; causes more or less circular,
slightly sunken lesions 1 to 6 mm. in diameter variously scat-
tered over the surface of tomato fruits, stems and leaves, being
characteristic on the fruits".
Existing confusion undoubtedly originated because of the in-
adequate original description. The binomial M. tomato Cke.
was correctly applied to the organism causing spots on tomato
fruits, later commonly known as nailhead spot, and should be
removed from the synonymy of A. fasciculata (C. & E.) J. & G.
as placed by Jones and Grout (41), and followed by Cook (20),
Butler (16) and others. Cultural studies have shown that M.
tomato Cke. occasionally produces spores in chains of two and
rarely three. But the fact that chain development does occur
is significant. Chain development of spores in nature has not
been observed and the usual spore types are long beaked.
Briefly summarized, the foregoing paragraphs show that nail-
head spot of tomatoes, as the disease is known today in the
southern United States, was originally collected in the south-
eastern United States by Ravenel and fungus was described by
Cooke in 1883 as Macrosporium tomato. Later this fungus,
through error, became associated with blossom-end rot of tomato
and those who studied the organisms associated with this phys-
iological disease concluded that it was a saprophyte. Further
consideration of the tomato diseases resulted in nailhead spot
being attributed to the early blight parasite. The type material
and other collections have been studied, from which it is con-
cluded that the fungus originally described as a parasite on
tomatoes is comparable with that causing nailhead spot in
Florida. In conformity with the above viewpoint based on
comprehensive studies, it is suggested that the name of the
nailhead spot-producing parasite be recognized as,
ALTERNARIA TOMATO (CKE.) n. comb.
Synonym-Macrosporium tomato Cke.
Grevillea 12:32. 1883.
The binomials Alternaria tomato (Cke.) Jones, which un-
doubtedly refers to the saprophyte Alternaria fasciculata (C.
& E.) J. & G., and Alternaria tomato (Cke.) Brinkman, because
it does not refer to the nailhead spot-producing parasite, as
intended, should both be dropped. The original description was
Nailhead Spot of Tomato
made from Exicc. No. 3099, and Ravenel's Exicc. No. 603 re-
sembles it very closely.
Type specimens--Ravenel's Collection No. 3099 at Kew.
Authentic specimens-Ravenel's Fungi American Exicc. No.
603. Kew.
North American Fungi Exicc. No. 2484.
S N. Y. Bot. Garden.
Numerous collections of nailhead spot on tomatoes, including
the material upon which this report is based, are deposited in
the herbarium of the University of Florida Agricultural Experi-
ment Station at Gainesville.
A description of the fungus as amended follows:
Spots circular to oval or irregular, shallow to sunken,
brownish-black on foliage, tan to brown on fruit, seldom over
a centimeter in diameter, amphigenous, irregularly scattered;
hyphae hyaline, branched, irregularly. septate, 4 to 10 t in
diameter, colonies grayish-white; conidiophores maculicole,
dark-brown, short, rigid, smooth, straight or curved, 3 to 8
septate, 7 / in diameter, 75 to 100 A in length, single or fas-
ciculate, bases swollen; conidia usually apical, dark, muriform,
obclavate, 51.87 x 14.74 A, 6 to 12 cross and 2 to 8 longitudinal
septations, terminating in an attenuate beak 82.16 p in length,
2 to 4 p in width, sparingly septate, sometimes forked; spores
usually borne singly, occasional 2-spored chains. On foliage,
stems and fruits of tomatoes, diagnostically characteristic spots
on fruit.
During the remainder of this paper the fungus will be re-
ferred to as Alternaria tomato (Cke.) n. comb.
Morphology.-Mycelium and conidiophores In nature the
mycelium appears superficially on diseased spots only after 12
to 18 hours of continuous high humidity. The spores germinate
quickly and in a few hours the fungus enters the host. After
penetration it spreads rather slowly, although growth is abund-
ant as far as it advances. It completely fills the intercellular
spaces in the invaded areas and penetrates the cell walls. The
total spread from any point of entrance in stems, foliage or
fruit is seldom greater than one centimeter, averaging about
half that distance.
In culture single, hyphal-strands are hyaline, while in colonies
the color varies from grayish-white to almost black. The
hyphae branch freely and are from 4 to 10 p in diameter, de-
Florida Agricultural Experiment Station
pending somewhat on the kind of medium on which they are
grown and on certain other cultural factors. Septations are
numerous and not regularly spaced. Their number is greater
per unit length of hyphae when the fungus is grown on a
medium low in nutrients. The contents of the hyphae grown
on a lean medium is also highly vacuolate when compared with
hyphae grown on 2 percent potato-dextrose agar. In old cul-
tures the imbedded hyphae often attain a much larger diameter
than normal and numerous septations divide it into chains of
round or oval, highly vacuolate, deeply pigmented, more or
less heavily walled cells.
In nature the conidiophores are maculicole, at right angles
to the surface of the host tissue. On the foliage they are at
first hypophyllous but as the spots become older they appear on
though they are
always more
abundant in pro-
tected areas or
where the humid-
ity is higher for
longer periods.
On fruit spots the
conidiophores ap-
pear first in the
central areas and
as the infection
becomes older
others develop
closer to the mar-
gin. The older
central groups
are often taller
and closer to-
gether than those
nearer the edge
of the lesions.
They are dark
brown, rigid,
smooth, 3 to 8
Fig. 8.-Characteristic conidia of Alternaria tomato two septate, straight
weeks old from tomato plants (6 left) and from culture (12
right) showing similarity except for length of beak. Or more or less
Nailhead Spot of Tomato
curved or angled, varying in length from 50 to 500 /A, averag-
ing 75 to 100 p, at first single, later fasciculate 1 to 12 together,
the center ones longer, bases are swollen and variously formed
when gregarious.
Conidia-As far as known the fungus produces but one spore
form, the conidia (Fig. 8). These are dark, muriform, atten-
uate beaked, obclavate or inversely club-shaped, the larger
portion attached to the conidiophore. In nature they are hypo-
phyllous and epiphyllous, caulicolous and fructicolous, being
least abundant on the foliage until after it has shed and most
plentiful on certain aged fruit spots. On the host the conidia
have always been observed to be produced singly, while in cul-
ture they may be found occasionally in chains of two.
The conidia themselves are exceedingly variable in size and
shape. Measurements of 100 conidia from fruit spots varied
from 39 to 65 p x 13 to 22 p, averaging 51.87 x 14.74 A. The
beaks averaged 82.16 / in length, and one of 100 spores con-
tained 4 longitudinal septations, 11 contained 3 septations, 8
contained 2, 40 contained 1, and 40 spores showed no distinct
longitudinal septation. All of the spores measured were mature
enough to germinate. Because of the difficulty in deciding
exactly where the spore proper ends and the beak begins, it
would be a miraculous achievement for two individuals to
measure conidia of a single species of Alternaria and show
less than 10 percent variation.
It is true that the body of the spore is usually dark. How-
ever, spores that will germinate are often very light yellow
and this color gradually blends from good visibility in the body
into the hyaline beak with no definite dividing line to separate
body and beak. The beaks also vary in length. They appear
to be shorter when developed during dry periods, and longer
when humidity is greater. In culture they show extreme de-
velopment, often a millimeter in length or 10 to 20 times as
long as the spore body. Rosenbaum (63) measured 500 conidia
in groups of 100'spores each and found the average dimensions
for these groups to be 55.2 x 17.2 p with the beaks 96.5 p in
length. (Fig. 9.) The variation between those reported by the
writer and those listed above may be wholly accounted for by
difference in maturity. Conidia of the nailhead spot fungus
will germinate before reaching maximum size and may become
exceedingly large, irregular in shape, almost black and opaque,
with an aggregate of 100 or more cells and 12 to 15 longitudinal
Florida Agricultural Experiment Station
septations. In contrast, 7- to 10-day-old conidia with dimen-
sions previously given and regular, light yellow to brown in
color, contain 12 to 20 cells and 1 to 4 longitudinal septations.
Elliott (30) places M. tomato Cke. in his "group 6", the meas-
urements of which are considerably less than for the Florida
fungus.
C
Fig. 9.-Copy of drawings by Rosenbaum (63) showing the nailhead spores at A, E, H and
early blight spores at B, C, F and G.
He showed in tabular form that 11 individuals engaged in
mycological work who gave measurements of a single Alternaria
spore, varied 8.5 percent in length and 30 percent in width,
and for many Alternaria spores on the same slide 41 to 43 per-
cent in extremes in length and 23 to 33 percent in extremes
in width. These data tend to convince one that spore measure-
ments should be used only as. an indication of a certain size
character and that other characters should carry more weight
than is usually given them in diagnostic uses in relation to
spores of certain fungi.
There is a particular uniformity in the profile of spores of
approximate age. As the spore matures and ages the ratio of
width to length steadily becomes greater, seldom if ever be-
coming equal, however. The transverse septations are usually
quite evenly spaced throughout the length of the spore. Occa-
Nailhead Spot of Tomato
sionally the septations closest to the apparent union of the body
and beak are more widely spaced than any other. The individ-
ual cells bulge slightly between septations, resulting in constric-
tions at the septa. In young spores the first cross septum
appears usually at or near the middle of the spore and additional
ones appear on either side of it. The longitudinal septations
do not appear until five to six cross septations have formed.
They appear first in the proximal half of the spore and later
in the distal half. The body of the spore is very distinctly and
abruptly tapered toward the beak. The greatest amount of
the change in diameter takes place in the body of the spore
rather than in the beak which is uniformly cylindrical. This
characteristic is unique with this fungus when contrasted with
closely related species that are parasitic on solanaceous plants.
The beaks average 2 to 4 t in diameter and are quite uniform
throughout their entire length, with rounded tip being slightly
larger where attached to the spore body. They are hyaline and
show few to many unconstricted septations. Usually the beak
septations are quite faint and indistinct, although with age
they become very numerous, prominent and show constrictions,
dividing the beak into several cells, each 2 to 3 times as long
as wide. The writer has observed forked beaks in about 1/10th
of 1 percent of spores examined. This is a rare occurrence
in contrast to the frequence of its appearance in certain other
Alternaria species.
Physiology.-The fungus grows well and sporulates in arti-
ficial culture. It has been grown on potato, prune, carrot, oat-
meal, malt and synthetic agars to which have usually been
added 2 percent sugar, most frequently dextrose. Best growth
is probably produced on potato-dextrose agar, although good
growth developed when maltose was substituted for dextrose.
The fungus was also grown on a nutrient agar prepared with
the standard ingredients, beef extract, peptone, and sugars.
Growth of the fungus on agar plates containing equal amounts
of dextrose, galoctose, lactose, maltose, mannose, raffinose and
saccharose showed that all of these sugars were beneficial as
compared with checks. Dextrose, saccharose and mannose were
best, the check (no sugar), raffinose and lactose showing the
scantiest growth. The mycelium is very dense, superficial,
clumpy, white to gray and covers the surface of the medium
in a common laboratory petri dish in about 10 days at average
room temperature. The medium is penetrated more or less
Florida Agricultural Experiment Station
by the fungus and appears to become bluish-black in color when
observed through the bottom of the culture dish after the cul-
ture is two or three weeks old. The color is darkest where the
hyphal growth is most dense. Frequently the fungus does not
cover the medium to the limits of the dish before the medium
becomes exhausted or stale. In such instances the margins of
the colony are quite transparent, whereas the central portions
of the plates are opaque. The growth of mycelium on these
clear marginal areas is scant and aerial, but it produces spores
abundantly. Growth is good on carrot and malt agars and only
fair on prune and synthetic media. Growth on clear, water-
agar is scant and almost invisible, but covers the entire plate
after several days at room temperature. Spores are produced
and show catenulation more often under these growing condi-
tions than on other media used.
When compared with many different closely related Alter-
naria spp., A. tomato should be considered as one sporulating
sparingly in culture. On potato-dextrose agar some spores are
produced during the first week, but they become more numerous
after the colony has covered one-half to three-fourths of the
surface of the culture dish. They are produced on hyphae-like
conidiophores that are slightly greater in diameter than the
hyphae from which they arise and usually they are darker
brown in color and appear to be more rigid. They vary in
length from one-fourth as long as the spore body to those a
millimeter or more in length. In young cultures spores are
scattered but later they appear to develop gregariously, result-
ing in certain aerial wefts of hyphae containing more than a
hundred conidia in close proximity. These clumps may be
widely separated by non-fruiting areas or where only a few
spores are seen.
By treating petri dish cultures of certain Alternaria spp. in
various ways they have been induced to sporulate more freely
than without such treatment. Rands (58) found that cutting
or shredding of 10- to 12-day-old potato agar colonies of A:
solani (E. & M.) J. & G. and slight desiccation and direct ex-
posure to the sun stimulated sporulation. Kunkel (43) observed
that M. tomato Cke. sporulated less freely than M. solani
E. & M., but that wounding of the hyphae in culture stimulated
it to produce conidia and conidiophores abundantly on different
media. Ramsey and Bailey (57) reported a definite stimulation
of spore production of the fungus which they designated as
Nailhead Spot of Tomato
M. tomato Cke. by ultra-violet radiation from a quartz mercury
arc between 2535-2800 Angstrom units, and also that filtered
sunlight in which rays lower than 3120 Angstrom units were
withheld likewise was favorable for abundant sporulation. The
writer found that cutting and shredding of the agar induced
abundant spore production and this method was followed
throughout the progress of these investigations to obtain
spores as needed.
.... -
Fig. 10.-Characteristic crystal formation produced on potato-dextrose agar by the nailhead
organism, viewed from the lower surface (left). Culture of early blight fungus (right).
The fungus growing at room temperature on 2 percent potato-
dextrose agar after several days produces a distinct, character-
istic type of crystalline substance that is imbedded in the medium
close to the glass surface (Fig. 10). It appears so regularly
and consistently that its appearance can almost be considered
a diagnostic cultural characteristic of the nailhead spot fungus,
since no other species of Alternaria or Macrosporium grown
on this agar has shown this substance. The crystals develop
from focal points and spread out fan-shaped in all directions.
-The denser vein-like development is light colored but opaque
and fine needle-shaped branches joining the main part at vari-
ous acute angles are fine in texture and resemble the pinnae
of a feather in their colonial relationship. These crystals are
produced plentifully after two weeks. The crystal groups are
discoid; when few and scattered they attain a diameter up to
one centimeter. When numerous and close together they aver-
age about a millimeter in diameter. The composition of these
Florida Agricultural Experiment Station
crystals has not been definitely determined, although they were
found to be insoluble in water, nitric, hydrochloric and sulfuric
acids and readily soluble in alcohol and potassium hydroxide
and their melting point is 249 C. They are probably an alkaloid-
glucoside combination, closely related to solanin, derived by the
action of the fungus on the carbohydrates and proteins from
the potato extract in the medium.
Germination of Conidia.-Conidia taken from spots on the
leaves and fruit or those grown in pure culture on artificial
media and placed in a drop of sterile distilled water on a glass
slide showed indication of developing germ tubes after 40 min-
utes at room temperature. When placed on the surface of
potato-dextrose agar in poured plates, germ tubes appeared in
less than an hour, thus indicating that germination takes place
rapidly in the presence of certain stimuli other than the host.
Normal germination occurs between 100 and 320 C. with 260
to 28 apparently optimum. Below 100 C. the rate of develop-
ment of germ tubes was considerably slower and at the higher
temperatures the development was accelerated up to 300 to
350 C., at which temperature germination was irregular and
abnormal. In germinating the spore swells slightly, causing
the constrictions at the septa to become more accentuated and
the outer cell walls between to become bulged. The episporium
is ruptured and the endosporium becomes immediately evident,
bridging the gap. It rapidly protrudes in parabolic form, ini-
tiating the germ tube which rapidly elongates from the tip and
forms a definite hyaline hyphal strand of uniform diameter,
filled with pseudogranular contents. No signs of germ pores
have been observed at any place on the spore wall of conidia of
any age. The spore will germinate apparently from any place
on its surface, including the beak. The cells in the middle of
the body of the spore germinate quickest under average condi-
tions, while the basal cells and those of the beak are much
slower. The germ tubes and young hyphae grow so rapidly
and branch so profusely that frequent observations are neces-
sary to follow the early growing habits of the fungus. How-
ever, it is doubtful if all the cells in any single spore germinate.
The cells in the beak of the spores have been observed to ger-
minate only. when the cells of the spore proper were mechani-
cally injured or when the beak was broken off from the spore.
The cells of the body of the conidia germinate independently
of each other, as was evidenced by the germination of isolated
Nailhead Spot of Tomato
cells in water. Spores were crushed and cut so that many
combinations of cells and portions of spores existed and only
injured or broken cells failed to germinate. Conidiophores and
mycelium, when cut and broken into small lengths, developed
new growth almost as rapidly as germinating conidia but it was
much less vigorous and at first usually of smaller diameter.
The new growth from these parts developed from the side or
either end of the broken filaments and usually from the conidia-
bearing end of a conidiophore.
Relation of Temperature and Light to Growth of the Fungus.
-Relation of temperature to growth of the fungus was studied
by growing the mycelium on poured plates of potato-dextrose
agar incubated at different temperatures. Equally small por-
tions of mycelium of the fungus from a common source were
transferred to the center of each plate and the plates were
placed in incubators at different constant temperatures and left
there until the colonies showing the fastest growth approached
the sides of the petri dish (Fig. 11, top). At 50 C. and below
the fungus survived but did not make any perceptible growth.
Below 150 C. growth was limited, and above this temperature
growth was successively greater up to 24 C., with the optimum
definitely between 24 and 270 C. At higher temperatures
growth was limited with little or no growth developing at 340 C.
At 360 C. growth was not only inhibited but the fungus was
killed after several days, as no growth took place when the
cultures were later incubated at the optimum temperature.
Light from various sources and of different degrees of in-
tensity apparently has little visible effect upon growth habits of
the fungus. The early blight fungus shows concentric zoning
probably caused by fluctuations in light intensity when grown
in culture on the laboratory shelves. The nailhead fungus has
not shown this character.
Growth of the Fungus in Relation to the Reaction of the
Medium.-The fungus was grown on potato-dextrose agar to
which different amounts of N/1 Hcl or N/1 NaOH were added
to adjust it to various pH reactions. The agar was prepared
at one time and made neutral to phenolphthalein, then 10 cc.
of the medium were placed in each test tube to which was added
one or more drops of N/1 Hcl or N/1 NaOH. Eight tubes
made up the series which was found by the use of the Youden
hydrogen-ion apparatus to range from pH 3.3 to pH 9. A num-
ber of series were made up, poured in petri dishes and inoculated
Florida Agricultural Experiment Station
Fig. 11.-The nailhead spot fungus in pure culture on potato-dextrose agar showing rate of
growth in relation to temperature (above), and to pH reaction of the medium (below).
Nailhead Spot of Tomato
with the fungus which developed from the same single spore
culture. These were incubated at room temperature. Several
other series were used to test the reactions of the. media at
the time of inoculation and from time to time during incubation.
The data were taken when the growth of the fungus in any
petri dish approached the edges of the container. The fungus
grew at concentrations ranging from pH 3.3 to pH 9.0, although
the growth at the acid end was barely discernible, while at the
alkaline extremity it was abnormal in color, texture and habit.
The optimum hydrogen-ion concentration for rate of growth was
on the alkaline side just past neutrality, although growth was
characteristic (Fig. 11, bottom) and very nearly equal in amount
and spread between pH 6.6 and pH 8.3.
Pathogenicity.-An anonymous writer (2) considered Macro-
sporium solani Cke. and M. tomato Cke. to be synonymous not
only for morphological reasons but because of favorable recipro-
cal inoculations in which these parasites from tomatoes and
potatoes were involved. Massee (50) also made similar experi-
ments with like conclusions. Brooks and Earle (13) frequently
found Macrosporium sp. on tomato fruits but the organisms
they isolated had always proven non-pathogenic. Butler (16)
attempted without success to infect tomatoes with Alternaria
fasciculata and A. solani. Rosenbaum (63) found that M. solani
E. & M. and M. tomato Cke. could be separated by differences
in infection obtained by inoculating tomato fruits. Only the
latter was pathogenic. Early leaf spots produced by the two
organisms were indistinguishable. He also stated that tomato
fruits under 6 inches in circumference were susceptible to in-
fection by the nailhead spot-producing fungus and easily in-
fected by inoculation without injury, whereas fruits of larger
size could not be infected by this method.
The writer has produced infection of tomatoes with numerous
cultures of the organism isolated in various ways, reisolated
the fungus from the diseased parts and verified the reisolated
organism by comparison with the originally isolated fungus.
Isolation.-The fungus was easily isolated from diseased
stems, petioles, peduncles, leaves and fruit of the tomato plant.
Diseased parts of the host were surface-disinfected and planted
on poured-agar plates. Growth appeared after 48 hours and in
72 hours it was sufficient to be easily transferred. The fungus
was isolated with least difficulty from diseased fruit. The fruits
were disinfected for 10 minutes in 1 to 1,000 corrosive sub-
Florida Agricultural Experiment Station
limate, washed in sterile water, opened aseptically and the inner
diseased tissue was removed and planted on hard-agar poured
plates. This procedure has almost always produced uncon-
taminated cultures of the parasite. Pure cultures of the organ-
ism have been obtained also by pouring dilution plates of spore
suspensions, from which single spores were transferred. These
transfers were made a few hours after germination had taken
place, at which time enough growth had developed to easily
locate the spore. The following quick method was used for
isolating single spores during most of the work: Conidia were
detached in large numbers from spots on fruits with a transfer
needle and allowed to fall by gravity onto the surface of hard
agar plates. They were located on the surface of the agar
through the inverted dish by the aid of a microscope and
permanently marked by a dot of ink on the glass. After 24
hours they were removed to other culture dishes.
Inoculation.-All inoculations were made by using sterile dis-
tilled water suspensions of the conidia that were developed either
on the parts of the host plant in nature or on artificial media
in the laboratory. The spores were taken directly from diseased
areas on leaves by excising them and washing the spores from
their surfaces. The leaf particles and other foreign material
large enough to clog a DeVilbiss atomizer were strained out
with a fine mesh screen. Spore suspensions were obtained by
scraping the spores into sterile distilled water from the surfaces
of diseased spots on fruits. Spores grown in the culture dishes
were loosened from the mycelium, which was first flooded with
water, with a sterilized camel's hair brush. The suspension
was strained from the petri-dishes into the container of the
atomizer. Viability of the spores used for inoculations was
always checked by making counts on hard-agar plates sprayed
in the laboratory with the spore suspensions previous to the
inoculation of plants. Tomato plants were always inoculated
in the series as a check on the pathogenicity of the fungus
whenever any other plants were being tested for susceptibility.
All plants were grown in the greenhouse and inoculated in all
stages of growth from seedlings to the time they were pro-
ducing fruits. Inoculation was usually accomplished without
mechanical injury. The plants were placed in a moist chamber
for 36 hours and then removed to a greenhouse bench at room
temperature (Fig. 12). The period from inoculation to spore
production varied from 48 hours to more than a week, usually
Nailhead Spot of Tomato
being about seven days. The production of spores on the host
plants was irregular and variable, depending primarily on hu-
midity. Continued low or continued high humidity was not
so conducive to
spore production
as periods of high "
humidity alter-
nating with
shorter periods
of low humidity.
The drying effect
on the fungus
appeared to aid
in abundant spore
production.
The plants used
for inoculation -
included species
of all the genera
of the Solanaceae
family occurring
naturally in Flor-
ida. In addition,
four cultivated -
varieties of Nico-
tiana tabacum~j.L
and 10 varieties
o f Lycopersicon Fig. 12.-Tomato leaf showing nailhead lesions resulting from
artificial inoculation.
esculentum were
used. The genus Solanum is represented by nine species, two
of which are cultivated. Results' of the inoculations given in
Table 1 show that horse nettle, (Solanum carolinense L.), egg-
plant, (S. melongena L.), and potatoes, (S. tuberosum L.) were
the only plants in addition to tomatoes (Lycopersicon esculen-
tum Mill.) that were susceptible to the disease, and these plants
were infected whenever inoculated except for certain tomato
varieties (Fig. 13, bottom). Some inoculated plants, such as
Solanum gracile, Physalis pubescens and Capsicium annuum,
showed very small flecks on the leaves in certain instances that
represented an effect of the fungus on the plants while they
were in the humidity chamber. Usually this type of flecking
did not continue development
to the greenhouse bench.
after the plants were removed
- I
Fig. 13.-Plants inoculated with spores from pure culture of A. tomato, showing relative
susceptibility. .Above: A. check; B, Earliana; C, Marglobe; D, Marvel. Below: A, check;
B, tomato; C, pepper; D, potato; E, eggplant; F, tobacco.
In addition to the plants contained in the following table
several species of plants in other families were inoculated.
These were selected because they grew in the tomato-producing
sections of the state that were suffering heavy losses from nail-
head spot. These were Sonchus oleraceus, S. asper, Mulgedium
floridanum, Bidens pilosa, Vernonia ovalifolia, Eupatorium sp.
and Ambosia elatior. In nature, all of them showed leaf spots
apparently caused by Alternaria sp. or Macrosporium sp. but
Florida Agricultural Experiment Station
Nailhead Spot of Tomato
none of them showed infection when inoculated with the nail-
head spot organism.
TABLE 2.-RESULTS OF INOCULATION EXPERIMENTS IN THE GREENHOUSE
IN WHICH SPORES OF THE NAILHEAD SPOT-PRODUCING FUNGUS WERE
ATOMIZED ON VARIOUS PLANTS.
i Number of Plants
Plant In- I Not In- I
oculated I Infected! oculated Infected
Physalodes physalodes (L.) Britt .... 10 0* 2 0
Physalis angulata L ........................ 10 0 2 0
Physalis pubescens L. ........................ 10 0 4 0
Androcera rostrata (D.) Rybd. ........ 10 0* 2 0
Solanum aculeatissimum Jacq. .......... 10 0* 2 0
Solanum bahamense L .......................... 10 0 2 0
Solanum blodgettii L ........................... 10 0 2 0
Solanum carolinense L ........................ 10 10 2 0
Solanum gracile Link. ........................ 23 0 4 0
Solanum melongena L. ......................... 34 34 10 0
Solanum sisymbrifolium Lam. ............ 10 0 2 0
Solanum tuberosum L. .................... 32 32 10 0
Solanum verbascifolium L. ................ 10 0 2 0
Perizoma rhomboidea (Hook) Sm .... 10 0 2 0
Lycopersicon esculentum Mill. ......... 70 60 20 0
Capsicium annuum L. ...................... 22 0 8 0
Lycium carolinense Walt. .................. 12 0 2 0
Cestrum nocturnum L. ......................... 12 0 2 0
Datura stromonium L. ...................... 10 0 2 0
Datura metel L ...................................... 10 0 2 0
Nicotiana tabacum L ............................ 70 0 10 0
Petunia hybrida Vilm. .......................... 8 0 2 0
*Certain flecking observed in moist chamber.
The host range of nailhead spot apparently is not great, at
least among the common species found in the Solanaceae family.
Horse nettle, tomato, eggplant, and potato were the only plants
that showed unquestionable susceptibility to the disease. The
diseased spots resulting from inoculations on these plants
showed certain common characteristics (Fig. 13). Other spe-
cies, namely Solanum aculeatissimum, Androcera rostrata and
Physalodes physalodes showed a definite flecking at various
times on the inoculated leaves several days after being removed
from the moist chamber but these miniature spots, often num-
erous, did not develop larger than barely discernible specks.
Consequently, they were not considered susceptible to the dis-
ease, although they were not as resistant as many other species
of the same genus that did not show any change following inoc-
ulation and incubation.
Plants of different ages were inoculated at different times
but only those that were susceptible, as shown in the table,
Florida Agricultural Experiment Station
became infected and usually regardless of age. Several series
of inoculations were made in which a portion of the plants
were more or less injured at the time the inoculum was applied.
The leaves were sprayed with the spore suspension until both
surfaces were thoroughly wet, and then they were gently rubbed
between thumb and fingers to break or otherwise injure the
trichomes but without crushing the leaf cells. Uninjured plants
were those not touched when inoculated. The plants that were
rubbed when inoculated usually developed 10 to 15 percent more
spots per unit area than the uninjured ones, but the injury did
not affect the incubation period.
.Other inoculation series were conducted in which several com-
mercial varieties of tomatoes were grown simultaneously and
inoculated at the same age with a spore suspension. All of these
varieties were placed in the moist chamber for a definite period.
The varieties inoculated were Marvel, Marglobe, Globe, Cooper's
Special, Magnus, Dwarf Champion, John Baer and Earliana.
In these tests the varieties were found to vary considerably
in degree of resistance, and they are listed above in the order
of their resistance (Fig. 13, top). The Marglobe was much less
resistant than the Marvel but more resistant than the Globe,
Cooper's Special, Magnus or Dwarf Champion. Earliana and
John Baer were both very susceptible and have been used in
all inoculation experiments to check the pathogenicity of the
inoculum.
Fruits of different sizes and ages were inoculated by atomiz-
ing spore suspensions over three-fourths of their surfaces and
by placing spores on the epidermis in definitely marked areas.
Both attached and detached fruits were inoculated by both
methods. The attached fruit and plants were kept in a moist
chamber for 36 hours and then placed on the greenhouse bench,
while the detached fruits were kept in a glass moist chamber
during the incubation period. Results obtained agreed with
those of Rosenbaum (63) in that small fruits were more sus-
ceptible than large ones, but disagreed in regard to fruits over
six inches in circumference being immune. The writer is more
inclined to accept the conclusions of Ramsey and Bailey (56),
who contended that nailhead spot develops on fruits of all sizes
but that the degree of susceptibility was correlated with age or
maturity of the fruit rather than size. In experiments recently
concluded all young fruits were susceptible and continued so,
regardless of size, until they reached a stage locally known
Nailhead Spot of Tomato
among growers as "mature green", at which time the skin of
the tomato becomes smooth and glossy in contrast to the rough,
dull skin of the immature fruit. Tomatoes begin to color shortly
after they attain the mature green stage.
FUNGUS AND HOST RELATIONS
Seasonal Development of the Disease.-Nailhead spot usually
appears annually with the tomato-growing seasons. It is found
during January in semi-tropical regions, such as Cuba and other
West Indian islands, Mexico, the Florida Keys and the frost-
protected parts of the Florida mainland. At this time the dis-
ease can be found on all ages of plants from those in seedbeds
to those that are fully developed and which have been picked
over many times and finally abandoned.
In Florida a few scattered summer plantings are often made
for early fall production, and on these the disease has caused
some trouble. The earliest plantings on a commercial scale
usually have been made about September 1 in southern Florida
for the Thanksgiving and Christmas markets. These fields have
been planted on "Pineland" soils because they are higher and
drier than the marl fields of the Everglade sections where the
major portion of the crop is planted later. These plantings
usually have suffered severely from the disease throughout their
entire existence and often have been abandoned after one or
two pickings because the disease has been so severe. This can
probably be accounted for because of heavy nightly dews and
high daily temperatures. Seedbeds in which the plants are
grown for the early part of the major producing season usually
are planted in October and November. Nailhead spot may ap-
pear on the seedling plants and continue to menace the crop
with increasing severity. Major production in the East Coast
section of southern Florida begins in February and continues
through March and into April. It is during this period that
nailhead spot has caused greatest damage to the crop in that
section. In the West Coast section the plants are set in the field
during the latter half of January and the first' part of February.
In this section the disease has caused injury to the young seed-
lings in the seedbed during January, and to transplanted plants
in the fields during February. The most damage from nailhead
spot during March and April has been reported from the West
Coast sections and during April and May from central Florida
areas, extending from coast to coast. The tomato season on
Florida Agricultural Experiment Station
the lower East Coast usually ends in April, the West Coast sec-
tion in May and the remaining Florida tomato-producing areas
in June. During June, July and August there have been few,
if any, commercial plantings of tomatoes in Florida, although
certain Gulf and South Atlantic states in former years have
produced them during early summer, at which time the disease
has occurred intermittently. It has seldom been found later
than July north of Virginia, Tennessee and Texas.
The writer has made no studies of the disease in transit.
However, Ramsey and Bailey (55) reported an increase in the
size of nailhead spots during six and one-fourth days in transit.
Longevity of the Fungus.-Spores produced on potato-dextrose
agar in the laboratory and kept at room temperature have re-
mained viable and showed very little or no weakening or delay
in germination after 18 months. The fungus remained viable
in diseased foliage and stems of tomato plants which were con-
fined in a burlap bag and kept out of doors at Gainesville from
the last of the growing season in June until the following April,
and caused infection on young caged tomato seedlings around
which the diseased material was banked. Caged and uncaged
check plants remained free from the disease. These experiments
supplemented by observations over a series of years are con-
clusive evidence that the fungus remains viable from season to
season in the fields, where tomatoes were infected previously.
In the past certain well located, highly productive lands have
been planted to tomatoes year after year without rotation.
Under these conditions the disease took an increasingly heavy
toll until finally these lands were abandoned entirely for tomato
growing. The disease has seldom been found on new lands
planted to tomatoes for the first time where strict sanitation
has been practiced, although it eventually has appeared. This
use of new lands continued until there were no longer desirable
new fields and as a consequence the total tomato acreage has
been reduced and other crops are being planted.
Source of Inoculum.-The fungus survives from one season
to another in old tomato stems, foliage and fruit skins left in
abandoned fields at the end of the picking season. In some loca-
tions the fields are often flooded by summer rains which kill
out all tomato plants, while in other cases some old plants sur-
vive and a second crop develops from seed of uncollected culls
at picking time. These plants become diseased and carry it
through the summer and up to the actual time work is started
Nailhead Spot of Tomato
in the fields for the next crop. Cultivation and plowing scatter
the spores over the surrounding areas. Unless a thorough job
of plowing is done not all of the old plants are covered and
any parts left exposed may continue to grow, harbor the disease
and produce spores.
Plants in seedbeds are usually growing in the vicinity when
operations for the next crop begin in these fields and it is prob-
able that plants in the seedbeds become infected by spores blown
from the fields. In other words, there is an overlapping of old
and young plantings that makes conditions favorable for propa-
gation of the disease. All early infections of commercial plant-
ings in the state probably originate in the immediate locality
from diseased plants of the previous season. This primary
infection may occur in the seedbed or after the seedlings have
been transplanted to the field. Seedbed infection naturally is
very much more serious than field infection because of the
possibilities of causing greater damage to plants and fruits
and also because of the possibilities of introducing the disease
into new localities. The primary infections of seedlings are
more important in relation to the secondary phase of the dis-
ease than the original sources of inoculum from which primary
infection occurred.
Spore Production.-Spores are produced in abundance in
nature on the surface of diseased areas on all parts of the
host plant above ground. They grow more profusely on the
nailhead-like spots on the green fruit than on any other part
of the living plant. The surface of fruit spots remains smooth
and shiny for about two weeks or until the fungus has pene-
trated beyond the cuticle and epidermis. When the, outer
parenchymatous tissue becomes invaded and moisture is lost
from it, the spot which previously appeared almost superficial
becomes depressed, and upon this sunken portion the conidio-
phores appear. They are usually short and quite centrally
located at first, appearing singly or several close together.
Others continue to appear on the perimeter of the diseased area
until the entire central portion is covered with them, the longest
ones being those that are oldest and centrally located. Conidio-
phores begin to produce conidia in abundance soon after their
appearance. After conidia become detached they may become
entangled with the conidiophores and form a more or less dense
mat. In such instances they become so abundant as to- give the
spot a black appearance. Conidia are produced continuously on
Florida Agricultural Experiment Station
these areas during the growing period of the host. Careful
observation has failed to reveal the conidia in chains over these
areas. They appear to become detached either because of nor-
mal abscission at maturity or by the development of other spores.
The former appears to be most logical since several scars are
discernible on some conidiophores which are apparently the
places of attach-
ment of conidia.
When conidia of
some Alternaria
S spp. are catenu-
S late the oldest
Sspore is attached
.- to the conidio-
phore, while the
o youngest is at the
S end of the chain.
Conidia are
S produced on stem
s lesions but not so
abundantly as on
fruit spots. Oc-
casionally, how-
--i ever, environ-
'.. mental and host
conditions are ap-
parently optimum
V-for their produc-
tion. Usually
these lesions are
Fig. 14.-Dead and withered leaf from tomato plant showing entirely barren
nailhead spots that killed it and now are producing spores in Of spores and co-
abundance.
nidiophores over
extended periods. This is because the fungus requires a longer
time to penetrate the epidermal layers of the stem and establish
itself in the more resistant parenchyma cells of the fibrous,
woody stems as contrasted with the more or less spongy tissue
of the fruit. Conidiophores and conidia are ultimately produced
on these invaded areas, however, in quantities sufficient to cause
a spread of the disease. They are not so concentrated in their
location on the stem as on the fruit and have never been ob-
served so dense as to change the color of the tan-colored spots.
Nailhead Spot of Tomato
On the foliage the disease spots may be few and scattered
or very plentiful. When few and scattered they may not seri-
ously affect the leaf except locally, and very few spores are
produced on the spots under these conditions. When the lesions
are numerous the invaded leaves turn yellow and die. During
the yellowing process and subsequent drying, conidia are pro-
duced in profusion, giving the spots a black color. The produc-
tion of conidia continues as long as moisture is retained in the
tissue. The leaves thus affected are usually shed and in the
presence of moisture on the soil surface become almost com-
pletely covered with a black, velvety layer of conidia (Fig. 14).
It is in this environment that the fungus may be mistaken for
any of several saprophytic forms unless carefully examined.
Spore Dissemination.-Conidia of A. tomato are borne on the
tips of conidiophores that project perpendicularly from the sur-
face of the affected tissue of the stem, leaf or fruit of the host
plant. This is conducive to easy detachment by the slightest
force and also to their dissemination. The long, slender beaks
apparently make the spores more subject to the influence of air
currents. In the air and in water suspensions the spores float
in a more or less vertical position with the beak uppermost.
When mechanically detached from the conidiophore and allowed
to drop 12 to 15 inches through a cylinder onto congealed agar
plates the. spores often come to rest in this vertical position.
In nature the spores are spread primarily by wind, rain and
running water, as well as by cultivators and pickers. Observa-
tions in Florida have shown that the disease has .been spread
from original foci of infection across fields in the direction of
prevailing wind. Whirlwinds often occur in tomato fields in
the state in which one can see plant refuse taken hundreds of
feet into the air. This agency could carry spores of the fungus
many hundreds of feet high and transport them for almost in-
definite distances. Stakeman (70) reports the trapping of
viable spores of Alternaria sp. 10,500 feet in the air. The con-
tinuous movement of plant parts by the wind is sufficient to
detach the spores. Examination of the surfaces of lesions for
the presence of spores reveals the fact that usually conidia are
found in abundance only in the areas definitely protected by
folded leaves and prominent veins. Rain and running water
are almost as important in local areas as wind in the dissemina-
tion of spores. Rain washes spores from affected plant parts
to uninfected parts and onto the soil or into accumulated puddles
Florida Agricultural Experiment Station
in the field. Surface water flowing to drainage ditches carries
the spores down the rows and through the fields, and raindrops
splash this surface water several inches in all directions and
in these ways the fungous spores are spread.
The spores are often unknowingly transported by the farmer
on diseased seedlings at transplanting time. Many fields in
distant locations might have been relatively free from the
disease in epidemic form if the seedlings had been free from
disease. Manns and Adams (46) attempted to obtain data on
the control of the disease on seedlings by dipping them in disin-
fectants before transplanting, but in their trials they reported
none of the disease on the checks. The spores are carried on
tools and implements used in cultivation, on the clothing of
workmen who cultivate the fields and on the hands of pickers
during harvest.
Time and Mode of Natural Infection.-Infection may take
place at any time on aerial parts of the host plant when en-
vironmental conditions are favorable. As previously stated,
moisture and temperature are important factors in spore ger-
mination and infection. Periods of high humidity due to fog,
dew, rain and cloudy weather provide favorable moisture. Spore
germination takes place at temperatures slightly above freez-
ing but the process is very slow until the temperature rises
to about 150 C. From this point up to 30 C. germination is
rapid and normal while above this temperature it is irregular
and abnormal or prevented. Under these conditions spores ger-
minate in from 8/ to 3 hours, and immediately following
germination infection is possible. Each spore may produce as
many as a dozen germ tubes, as each cell of the spore possesses
the potential ability to produce a germ tube. However, during
these studies the germination of every cell in a spore has not
been observed. The tubes lengthen rapidly, branch profusely
on artificial media, much less on the host, and enter the host
directly or through the stomata. Penetration at night is not
as frequent under highly humid or saturated conditions as when
less moisture is present. Under conditions of low humidity
mycelial growth is almost stopped and the relative amount of
penetration is negligible, although the fungus is not killed.
Under Florida conditions the humidity is seldom so low at night
as to prevent spore germination and host infection. The spores
will survive and germinate under low temperatures that do not
kill the host plant. Likewise, they will germinate and infect the
Nailhead Spot of Tomato
host during night temperatures under the warmest Florida
weather conditions. Temperature and humidity, individually or
in combination, more or less regulate the mycelial growth on
the surface of leaves of the host. Under favorable conditions
over an extended period the mycelium from a single centrally
located spore may extend in all directions to the edges of a
tomato leaf and penetrate the leaf tissues in only a few scat-
tered places. With less favorable conditions the length of
mycelium may be limited to a few millimeters with abundant
penetration. There seems to be no obstacle on the part of the
host to prevent penetration, neither has there been observed
any specially developed apparatus on the part of the fungus to
insure penetration. The mycelium grows over the surface of
the host tissue at random during high humidity and follows
the creases formed above the contacting walls of adjacent
epidermal cells more often when the humidity is low.
Period of Incubation and Pathological Anatomy.-Following
penetration, growth of the fungus within the host is dependent
apparently only on temperature in susceptible plants. Conidia
transferred without moisture from diseased spots to dry living
tomato leaves exhibited no tendency toward germination for
at least 12 hours, whereas conidia transferred from the same
lesions and placed on wet living tomato leaves showed germ
tubes within one hour. Penetration of the host takes place any
time after germination. The absorption of plant juices and
resulting weakening and starving of the host cells may, in a
small way, contribute to their death. It is apparent, however,
that the far more important factor in their death is the influence
of certain exudates by the fungus, such as exzymes or toxins
which are exceedingly detrimental to the host cells and kill
them very shortly after contact is made. This rapid action
results under favorable conditions in the killing of enough host
cells within 36 to 48 hours to form a small discolored area
visible to the unaided eye. This is the first symptom of the
disease. Under field or unfavorable conditions, the period from
inoculation to the first indication of killed host cells may cover
a week or 10 days. Usually, however, this time is from three
to five days. Following this first symptom, the lesion, consist-
ing of dead cells, enlarges rapidly until the spot is half a centi-
meter in diameter (Figs. 15, 16). It is visible almost from the
first from both sides of the leaf, indicating that the fungus
grows through the leaf and ramifies in all directions. The killed
46 Florida Agricultural Experiment Station
Nailhead Spot of Tomato
Fig. 15.-Series of photomicrographs showing pathological anatomy of the nailhead spot
disease on tomato fruits, stained with a modified Pianese 3b, magnified 150 times.
A, Section of disease-free fruit tissue, showing from top to bottom, cuticule, epidermis,
4 to 5 layers of small cork cells, 10 to 12 layers of cortex cells, clump of vascular tissue,
3 to 6 layers of large spongy parenchyma cells, 1 to 2 layers of small parenchyma cells
and a single layer of small cells that form the lining of the seed locules.
B, The dark stained area has been invaded by the parasite.
C, The larger stained area shows an older infection, resulting in the loss of contents
of the larger cells.
D, This radial section shows a dark stained fungus-invaded area with large empty cells
contrasted to the uninvaded nucleated cells. The sunken nature of the diseased area results
from the rapid collapse of the 4 to 5 layers of small cork cells just beneath the epidermis.
E, Cross-section of an old fruit lesion showing scattered conidiophores of the fungus
protruding from the surface.
cells are invaded rapidly by the fungus, become dry and turn
brown. The margins of the spots show the fungus hyphae in-
vading the host tissue between the cell walls, although soon
after contact the cells are weakened and killed so that extensive
development of the fungus in living host tissue does not occur.
The enlargement of the lesions can be correlated with humidity.
The higher the humidity the larger the spot becomes within
certain limitations. Following death the cells dry out and as
the central portions of the spots dry the rate of increase in
size of the spot diminishes until an apparent balance is reached.
Conidia are produced on the central part of the spot about the
time it ceases to enlarge and their production may reduce the
Florida Agricultural Experiment Station
Nailhead Spot of Tomato
Fig. 16.-Series of photomicrographs showing pathological anatomy of the nailhead spot
disease on stem and leaves of tomato plants, stained with Pianese Sb, slightly modified.
A, Cross-section of portion of a tomato stem showing the dark stained, infected area
which includes the epidermis and cork cells of the cortex, which are collapsed, being limited
to the tissue outside the vascular ring (x 50).
B, The early infection of leaf tissue by the fungus is shown by the dark stained portion.
The fungus has invaded and ruptured the epidermis and is beginning to penetrate the upper
portion of the palisade cells (x 150).
C, Leaf infection further advanced than above; the hyphae of the parasite have pene-
trated the leaf to the lower surface and they are shown occupying the intercellular spaces
over an extended area (x 150).
D, An advanced stage of the disease showing the cross-section of a leaf spot sunken
from both surfaces because of collapsed host cells. The fungus apparently kills the host
cells rapidly, as revealed by the sharp demarcation between uninvaded and invaded host
tissue (x 150).
E, Demonstration of the hyphae of the fungus inter- and intra-cellularly (x 400).
vitality of the fungus so much that its extension is slowed
down or even stopped. Again, the leaf may be weakened by
the parasite and less food material is supplied or autolysis may
take place, resulting in spore production as a natural tendency
of survival.
A single lesion on a leaf blade unless located on one of the
principal veins will not cause the leaf to shed, except under
most favorable conditions. On the other hand, relatively few
lesions may cause rapid and almost complete defoliation. After
the whole leaf has been killed and begins to dry, conidia are
produced abundantly. If the leaf falls to the ground where
there is plenty of moisture and long periods of high humidity,
50 Florida Agricultural Experiment Station
the hyphae of the fungus grow over both surfaces of the blades
and conidia are produced so profusely that the leaf appears
blotched with black.
Under the most favorable conditions the first mature spores
may appear six to eight days after inoculation; under average
field conditions, this period is usually lengthened to 10 to 14
days. The early production of spores is not plentiful and one
often experiences difficulty in finding them. On the other hand,
spore production on the fruit after two weeks is abundant while
on the fallen leaves spores are produced in such quantities as to
give them a fuscous appearance.
SUMMARY
1. Nailhead spot of tomatoes, known in Florida for the past
25 years, has caused millions of dollars worth of damage to
the crop in Cuba, West Indies, Mexico and southern United
States.
2. Its host range consists of tomato, potato, eggplant and
horse nettle.
3. All phases of the disease are described.
4. The causal fungus has been transferred from the binomial
Macrosporium tomato Cke. to Alternaria tomato (Cke.) n. comb.,
and existing errors recorded in literature concerning the disease
it causes are pointed out.
5. Certain physiological and morphological characteristics of
the fungus are discussed along with the seasonal development
of the disease in nature and through inoculation experiments.
6. Pathogenicity of the parasite has been proved and patho-
logical anatomy of the disease demonstrated and explained.
Nailhead Spot of Tomato 51
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