48 FLORIDA STATE HORTICULTURAL SOCIETY, 1974

CHARACTERISTIC INJURY BY CITRUS RUST MITE

TO ORANGE LEAVES AND FRUIT

L. G. Albrigo and C. W. McCoy Materials and Methods

I FAS Agricultural Research and Education Center
Lake Alfred
Abstract Frequent probing of upper and lower
leaf or fruit surfaces by the citrus rust mite,
Phyllocoptruta oleivora Ashmead, caused subse
quent epidermal cell lignification and browning.
Extensive lower leaf surface injury resulted in
mesophyll collapse adjacent to the epidermis. Sub
sequently, a wound periderm formed between
healthy and collapsed mesophyll cells. The more
pronounced injury to the lower leaf surface may
be due to loss of stomatal control of transpiration.
In the grove, mite populations reached higher
densities on the fruit as compared to leaves, this
being a probable explanation for the lower inci
dence of leaf to fruit injury. Characteristics of
injury to fruit previously referred to as "shark
skin," "buckskin," "russet" and "bronzing," "early
rust mite injury," and "late rust mite injury" are
Leaves with rust mite injury were collected in
1973 and 1974 in groves harboring high mite
populations. Cross sections of leaves were im
mediately cut (24 to 36 fim thick) on a Hooker
plant microtome for histochemical and microscopic
examination. Sections were stained 1 hr with sat
urated phloroglucinol in 20% HC1 for lignin, or
1/2 hr with saturated sudan III in 70% ethanol
for lipids followed by 5 to 10 min in a 50% ethanol
wash (4).
In 1972-73, mites were monitored bimonthly
in a Polk County grove on both leaves and fruit
by counting the number of mites on 45 fruit from
April 1 through May 5, 1972 and 15 fruit there
after (until April 1973) and 120 leaves. At peak
mite density, the surface area of fruit and leaves
was estimated and mite density for given surface
area calculated.
Results and Discussion

explained in light of new findings on rust mite in

Rust mite injury was found on both surfaces
jury. Variations in leaf and fruit injury patterns
of orange leaves. Lower surfaces often showed
caused by plant anatomy and growth character
"leaf mesophyll collapse," appearing first as yellow
istics are discussed.
degreened patches and later as necrotic spots
(Fig. 1, A and B). Lower leaf surface injury
Recent work has shown that injury to the fruit sometimes stopped with browning of the epidermal
caused by citrus rust mite feeding is restricted to cells. Injury to the upper leaf surface appeared as
epidermal cells (4). When multiple feeding and/ small brown spots or blotches (Fig. 1, C and D).
or probing punctures occur within a short time on Upper leaf surface injury has been reported to
a given cell, the cell produces lignin and subse result in bronzing and russeting (rough upper
quently dies. When injury occurs before fruit surface) symptoms (11).
maturity, further fruit growth leads to a break Leaf sections taken from areas showing meso
ing up of the dead epidermis and subsequent phyll collapse stained for lignin with phlorogluci
wound periderm formation beneath the epidermis. nol and showed that cell damage extended into
No wound periderm forms when injury occurs late several cell layers (Fig. 2A). Discoloration of the
in the season after fruit has reached maturity. epidermal cells appeared earlier and was more
Although visible injury to fruit is more com uniform than darkening of the underlying cell lay
mon, leaf injury can occur (3, 7, 11) and occasion ers. Often damaged, cells were separated from
ally is severe (3). Extensive leaf injury has been healthy leaf tissue by a wound periderm which
reported as "mesophyll collapse" on the under stained for lipids with sudan III (Fig. 2, B and
surface (7) or "russet" of one form or another C). When the injured areas showed considerable
on both leaf surfaces (11). In this paper, new in necrosis, the lower cuticle tended to separate from
formation on citrus rust mite injury to leaves and the healthy upper area indicating that injured
fruit of orange is presented in light of further areas were no longer cohesive (Fig. 2D). Both
field observation and histochemical study. injury to fruit (russet) and leaf "mesophyll col
lapse" resulted in a wound periderm, but in the
case of leaf injury several cell layers were dam
Florida Agricultural Experiment Stations Journal Series
No. 5654.
aged. The intense leaf injury to the lower leaf
 ALBRIGO & MCCOY: RUST MITE INJURY 49

Fig. 1. A. Leaf showing 'mesophyll collapse' from rust mite injury. B. Close-up of necrotic areas within chlorotic patch. C.
Upper leaf surface 'bronzing' from rust mite injury. D. Close-up of 'bronzed' patches.

surface was probably caused by destruction of Generally, injury to the leaf occurs less fre
stomatal guard cells. The lower leaf surface could quently than injury to fruit. In the 1972-73 season,
not control water loss after death of these epi rust mite populations on the fruit were consider
dermal cells. Subsequent water stress would lead ably higher than on leaves (Fig. 3). The peak
to damage of the loosely packed and exposed mite mean densities/cm2 were 1.4 and 47.6 mites
mesophyll cells near the lower surface. The fruit for the leaves and fruit, respectively. Lower pop
surface has considerably fewer stomata than the ulations on the leaves probably account for the
lower leaf surface and the subepidermal cells in lower incidence of leaf injury. It should be pointed
the fruit are tightly packed. Growth stress is out that neither of these mean peak densities were
probably the major factor causing wound periderm high enough to cause epidermal cell injury (4).
formation in the fruit (4). Since mites tend to aggregate (4), probably as a
Mite injury to the upper leaf surface was lim result of more favorable microclimate or feeding
ited to epidermal cells (Fig. 2, E and F) that conditions, injury areas usually correspond with
stained for lignin with phloroglucinol. No wound mite aggregation. Also, leaves may develop less
periderm formed below the injured upper surface, rust mite injury than fruit because epidermal cell
probably because no internal stress occurred fol water loss from heavy mite feeding presumably
lowing rust mite probing. The absence of stomata could be replaced more rapidly in the leaves. This
on the upper leaf surface and the tightly packed is because citrus leaves can replenish some of their
palisade parenchyma cells under the epidermis moisture loss at the expense of the fruit (2).
will prevent development of appreciable water Although initial injury to the epidermal cells
stress. Internal stress from cracking of dead of leaves and fruit appear to be similar, changes
epidermal cell areas will not occur unless rust mite relative to fruit growth and maturation can alter
injury occurred during leaf expansion. final appearance considerably. Several factors can
50 FLORIDA STATE HORTICULTURAL SOCIETY, 1974
 ALBRIGO & MCCOY: RUST MITE INJURY 51

influence final injury appearance. Differences in
plant structure of the injured area, one of these
factors, results in more extensive injury to lower
than to upper leaf surfaces (see preceding text for
details). In fruit, the stage of development when
initial injury occurs is very important in determin
ing the final appearance of the injured area. This
factor accounts for the primary types of rust mite
damage recognized on fruits.
"Early rust mite injury" to oranges has been
distinguished from "late rust mite injury" on the
basis of a rough cracked ("russet") or smooth
("bronze") surface at time of harvest (3).
Actually, three known visible types of fruit in
jury can develop depending on variety or stage of
fruit development at the time of initial injury;
namely "sharkskin," "russet," and "bronzing."
"Sharkskin," recognized as occurring on grape
fruit, lemons, and limes (3, 11) can occasionally
develop on oranges (Fig. 4A). When the epidermis
is damaged severely at an early age, further fruit
growth results in a cracking of the dead epidermis
in patches (Fig. 4B). These eruptions may slough
off, leaving a smooth injured surface area (wound
periderm) or remain on the surface when injury
occurs later. Some fruit injuries classified as
"buckskin" in the grade standards for Florida
citrus (8) are the result of early rust mite injury.

3,810.2- 476 MITES PER CM2

100- 2500

1.4 MITES PER CM2

80 2000

60 1500
• • LEAF tr.
UI
o o FRUIT Q.

UJ
UI
1000 t

or
UJ
UI
CD
m
2
20 500

APR MAY JUN'JUL'AUG'SEJ DEC'JAN FEE MAR APR

1973
Fig. 3. Changes in leaf and fruit surface populations of citrus rust mites during the 1972-73 season. Average counts on
120 leaves and 45 (April 1 thru May 30, 1972) or 15 (June 1, 1972 thru April 1, 1973) fruit on each date in a Polk County
'Valencia' grove.

Opposite

Fig. 2. Cross sections of leaves showing lower leaf surface 'mesophyll collapse' (A-D) and upper leaf surface 'bonzing'
(E-F) representative of citrus rust mite injury. A. Extent of damaged area (100X); B. Wound periderm separating damaged
and healthy mesophyll (100X); C. New periderm cells, walls stain for lipids (400X); D. Older mesophyll collapse with dis
rupted area (100X); E. Upper leaf surface epidermis damage (100X); F. Close-up of upper leaf surface 'bronzing' showing
darkening of cell contents (400X).
52 FLORIDA STATE HORTICULTURAL SOCIETY, 1974

Fig. 4. Appearance of sharkskin (A and B), russet (C and D), and bronzing (E and F) rust mite damage on oranges. The
damage conditions as they appear on whole fruit (A, C, and E) are respectively shown (see arrows) in cross sections of the
peel in plates B (100X), D (100X), and F (400X).
 ALBRIGO & MCCOY: RUST MITE INJURY 53

"Husset" condition of orange (Fig. 4C) de
velops when rust mite injury occurs before the
fruit have obtained their full size, late spring
through early fall (4). Cracks develop in the
epidermis and a wound periderm forms from con
tinued growth stresses (Fig. 4D), but the epi
dermal layer does not break up into separate
patches. The cracks result in a rough texture
which cannot be polished, while the oxidized cell
contents give the fruit their brown color (4).
''Russet" is also a grade standard for Florida
citrus (8).
Fruit "bronzing" (Fig 4E) occurs from initial
rust mite injury at a time when little additional
fruit growth will take place (late fall). Epidermal
cells die and become brown, but the cuticle does not
develop cracks (Fig. 4F). Unlike "russet" or
anges, these fruit will polish since the natural
cutin and wax layer is not broken up. These fruit
are referred to as "bronze" in the grading stand
ards for Florida citrus (8).
Two factors can alter the development of these
basic injury patterns. Fruit injured by rust mites
in early, mid, or late stages of growth and de
velopment will have "sharkskin," "russet," or
'bronzing" injury symptoms at harvest. Growth
and development of the fruit is a gradual process
and so is the change from developing one injury
symptom to the next (e.i., a mite infestation in
midspring will result in damage that shows some

Fig. 5. Variations of citrus rust mite damage to oranges. A. Rust mite damage around a sun spot area which was unin
habited by rust mite; B. C^H degreened zone (between arrows) from mite injury around a sun spot, slightly earlier damage
beyond has browned; C. Chimera on fruit with less rust mite damage than surrounding tissue; D. Chimera with more dam
age than surrounding tissue.
54 FLORIDA STATE HORTICULTURAL SOCIETY, 1974
"sharkskin" characteristics and some "russet" ap
pearance). The other factor concerns the amount
of the total epidermal cell population damaged. If
all epidermal cells are damaged within a given
area, final appearance of injury will depend on
the stage of fruit development at the time
initial injury. However, if a number of epidermal
cells are left undamaged in the injured area, more
cells are left to divide and enlarge,
alleviating much or all of the stress on the epi
dermis caused by subsequent fruit enlargement.
In this case, severity of the appearance or in
jury will be lessened.
Other variations of mite injury patterns were
observed to relate to mite distribution and fruit
growth and development. In the spring, mites on
young fruit may aggregate in surface depressions
particularly on rough surface varieties such as
"Valencia." These depressions presumably have a
more favorable microclimate for mite habitation.
In some of the depressions, clusters of browned
(damaged) epidermal cells were observed. Rust
mites do not inhabit sun exposed fruit surfaces.
However, damage often occurs around the edge
of the sun spot where mites tend to aggregate
(Fig. 5A). These sun spot damage patterns were
observed during summer and fall.
In summer and fall, intense rust mite feeding
can also lead to bleaching of the epidermis. The
injured areas take on a whitish cast and some
times no subsequent browning occurs. It was not
determined whether the cell contents were sub
stantially removed by rapid mite feeding or the
surface was punctured to the extent that no con
sistent path for light reflection remained. Loss of
cell contents seems likely, at least, in cases where
nc subsequent browning occurred.
Some variation in mite injury patterns is af
fected by characteristics of the fruit. Degreening
of injured areas was observed before cell brown
ing took place on mature "Hamlin" fruit in the
fall when chlorophyll was sensitive to ethylene
(C2H4) degreening (4). This characteristic
shown around a sun spot in Fig. 5B. Fruit surface
strips developing from genetic mutations
meras) can be less (Fig. 5C) or more (Fig. 5D)
susceptible to rust mite injury than the normal
surface. The mutations either change
susceptibility to injury or the cell suitability for
mite feeding (4).
Some confusion has existed in the literature
concerning the possible role of citrus, rust mite as a
secondary factor in "greasy spot" disease (3, 5)
and the possible role of Cladosporium
atrum McAlp. in "russet" formation (1, 6). The
mode of infection for "greasy spot" has been
studied in detail (9, 10). It appears that punc
tures to the leaf surface caused by rust mite could
not serve as a mode of entry for this disease since
of the "greasy spot" organism, Mycosphaerella citri,
penetrates through stomata only and initially
grows in the intercellular spaces around the
therefore, spongy mesophyll cells.
C. brunneo-atrum was found in "russet" areas
of mature fruit (1) and was presumed to be re
lated to russeting because certain spray treatments
reduced "russeting" and were known to be fungi
cides (1, 6). The examinations for fungi were
made considerably after "russet" first appeared.
In recent work on rust mite damage (4), no fungi
were observed in injured areas until after cuticle
cracks were present. These fungi did not penetrate
the wound periderm already formed below the
epidermis. Mycelia were always found first in the
subepidermal cell area along the cuticle cracks.
These fungal growths were apparently secondary
invasions since they were always found inhabiting
this dead tissue area.
Although the visible injury caused by the citrus
rust mite takes on many patterns, the feeding by
the mite is restricted to the epidermal cells and
can directly result only in lignification and death
of these epidermal cells. The variations observed
are caused primarily by differences in stage of
fruit or leaf development when injury occurs or
structural differences of the damaged epidermis
or the tissue beneath. These factors lead to various
physiological stresses subsequent to the initial mite
damage. Intensity of initial epidermal cell injury
seldom plays a role in the variability of rust mite
injury patterns.
Literature Cited
1. Fisher, F. E. 1957. Control of citrus fruit russet in
Florida with Zineb. Phytopathology 47:433-437.
2. Furr, J. R., and C. A. Taylor. 1939. Growth of lemon
fruits in relation to moisture content of the soil. U.S.D.A.
Tech. Bui. 640:1-72.
is 3. Griffiths, J. T., and W. L. Thompson. 1957. Insects
and mites found on Florida citrus. Univ. Fla. Agr. Expt.
Sta. Bui. 591:39-42.
4. McCoy, C. W., and L. G. Albrigo. 1974. Feeding be
(chi havior and nature of injury to the orange caused by citrus
rust mite. Phylloeoptruta oleivora (Prostigmata: Eriophy-
oidea). Ann. Entomol. Soc. Amer. (in press).
5. Muma, M. A. 1975. Contemporary and potential control
of injurious insects and mites on Florida citrus. Proc. Tall
the cell Timbers Conf. on Ecol. Animal Control by Habitat Manage.
No. 6 (in press).
6. Puzzi, D., and H. V. de Arruda. 1964. Correlacao entre
niveis de infestacao do acaro Phylloeoptruta oleivora (Ashm.)
e a ocorrencia das muchos da "ferrugem" dos citros (in
Portuguese). Apr. Inst. Biol., Sao Paulo. 31(4) :167.
7. Thompson, W. L. 1946. Preventative sprays for mite
control on citrus. Proc. Fla. State Hort. Soc. 59:60-65.
8. U.S.D.A., Agr. Marketing Service, and Fla. Dept. Agr.
and Consumer Services. 1973. U.S.D.A. official visual aids for
brunneo- Florida citrus. The John Henry Co., Lansing, Mich. 75 p.
 HUTCHESON & BELLIZIO: DRIP IRRIGATION SYSTEMS 55

9. Whiteside, J. O. 1972. Histopathology of citrus greasy fection of citrus leaves by Mycosphaerella citri. Phytopath-
spot and identification of the causal fungus. Phytopathology ology 64:115-120.
62:260-263. 11. Yothers, W. W., and A. C. Mason. 1930. The citrus
10. . 1974. Environmental factors affecting in- rust mite and its control. U.S.D.A. Tech. Bui. 176. 56 p.

A SURVEY OF DRIP IRRIGATION SYSTEMS

IN SOUTHWEST FLORIDA1

C. E. HUTCHESON to measure water quality and compare the informa

tion with emitter plugging, flow rates, and meth
IFAS Cooperative Extension Service
ods used in operating the systems. The systems
Arcadia
surveyed were also compared to optimum water
and outputs suggested by Myers and Harrison (4).
Blackwell has previously reported on one of the
J. E. Bellizio systems observed (1).

IF AS Cooperative Extension Service

Naples Materials and Methods

The area covered by the 10 systems observed

Abstract Ten drip irrigation systems in Col
was 440 acres with 80 percent using micro or
lier, Hendry and Lee Counties were surveyed to
spaghetti type tubing, 6 percent lines with open
compare and evaluate water sources and quality,
holes, 5 percent take apart emitters and 9 per
operating procedures and problems, and types of
cent push button type systems (Table 1).
emitters. Irrigation water was obtained from
Water quality and pH were measured in the
wells and ditches. Three of the four systems using
field with a Hach Model DR-EL Portable Water
filters had installed them after emitter plugging Engineer's Laboratory kit.
occurred. Four emitter types were observed. Flow
Measurements included pH, total iron, using
rates ranged from 0.5 gal/hr/tree to 6 gal/
the 1,10-phenanthrolin method, hydrogen sulfide
hr/tree. Water samples tested for iron ranged
by the lead acetate method, and dissolved oxygen.
from 0 to 1.5 mg/1, and hydrogen sulfide from 0 Water samples were taken at the water sources
to 5 mg/1. Both substances appeared to be as
(before the sand or screen filter) an at the
sociated with plugging. Systems operated from a
terminus of the emitter lines. If systems were not
few hours a day on new plantings to 24 hours a in operation, they were turned on and allowed to
day on older plantings. While most systems had stabilize before water samples were taken. Rates
numerous emitters plugged, no trees were in a
of flow were recorded at functioning emitters se
wilted state during an extended drought period. lected at the beginning, middle and end of lines.
The water quality of the filtered systems was
The water needs and the economics of ir compared to that of the unfiltered to determine
rigating citrus have been shown in Florida (3). any effect on emitter function.
Irrigation of citrus in flatwoods groves has been Tree canopy measurements were made. Theo
profitable due to shallow root zones and low soil retical water needs were then calculated for trees
water holding capacity. The increasing costs of this size. This need was then compared to the
irrigation systems and the high water consump actual amounts of water the trees were receiving.
tion have stimulated interest in drip irrigation
systems. Approximately 1500 acres of drip ir Results and Discussion
rigation have been installed in citrus groves in the
3 counties surveyed. The purpose of this paper is All drip irrigation systems studied in the
survey had been operating less than 24 months.
With only 2 exceptions, all systems had approxi
lThe authors express appreciation to Drs. H. W. Ford and
D. P. H. Tucker at the AREC, Lake Alfred for their con mately 25 to 50 percent of the emitters that were
structive comments and suggestions in carrying out this
survey and compiling the results. not functioning. One exception was system 7 which