Ecology and Aerobiology of Dispersing Citrus Rust Mites (Acari: Eriophyidae) in

Central Florida
Author(s): J. C. Bergh
Source: Environmental Entomology, 30(2):318-326. 2001.
Published By: Entomological Society of America
DOI: http://dx.doi.org/10.1603/0046-225X-30.2.318
URL: http://www.bioone.org/doi/full/10.1603/0046-225X-30.2.318

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 POPULATION ECOLOGY

Ecology and Aerobiology of Dispersing Citrus Rust Mites

(Acari: Eriophyidae) in Central Florida
J. C. BERGH1
IFAS, Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL 33850

Environ. Entomol. 30(2): 318Ð326 (2001)

ABSTRACT Aerial dispersal of citrus rust mite, Phyllocoptruta oleivora (Ashmead), in central
Florida showed a diel periodicity peaking between late morning and early afternoon. The abiotic
factors that best described the dispersal pattern were solar radiation, time, and leaf wetness; whereas
wind speed, humidity, temperature, and rainfall had minimal effect. The longevity of adult mites
removed from fruit was inversely related to constant temperatures between 25 and 35⬚C. The
longevity of mites removed from fruit at 2-h intervals between 0700 and 1300 hours and exposed to
ambient temperature and humidity outdoors was inversely related to the time of removal from the
host. There was a linear relationship between the number of mites captured in traps and population
density on fruit. Mites left fruit harboring extremely low populations and some fruit supporting dense
populations yielded hundreds of dispersing mites per day. Mites were readily carried on air currents
between adjacent citrus groves. Nearly all of the mites captured in dispersal traps were adult females,
and were found in greater proportions in traps than would be expected from the sex ratio of mites
on fruit. Studies using isolated fruit in the laboratory showed that a single virgin or inseminated
female could initiate a local population through oedipal mating and sibmating. The data are discussed
in relation to the selective forces that may shape the dispersal behavior of citrus rust mite and to the
potential impact of aerial dispersal on mite management and the development of acaricide resistance.

KEY WORDS Phyllocoptruta oleivora, dispersal, traps, mite management

CITRUS RUST MITE, Phyllocoptruta oleivora (Ashmead),
is a key pest of citrus grown in humid climates. Cu-
mulative feeding on the surface of fruit by P. oleivora
results in cosmetic damage and rejection of fruit for
the fresh market. In Florida citrus, the majority of
pesticide applications each year are for management
of this mite.
Colonization of new citrus hosts by P. oleivora is
primarily by aerial dispersal (Bergh and McCoy 1997).
Like other eriophyid species (Sabelis and Bruin 1996),
adult citrus rust mites exhibit dispersal behaviors, in-
cluding standing erect on their caudal lobes and leap-
ing, which are thought to elevate them above the
boundary layer within which they live (Frost 1997).
Mites that release their hold on the host plant are
borne away on air currents and can be captured in
traps (e.g., Slykhuis 1955, Nault and Styer 1969, East-
erbrook 1978, Bergh and McCoy 1997).
Most eriophyid mites, including citrus rust mite, are
host-speciÞc (Cromroy 1979). Although mites ac-
tively initiate dispersal, once aloft, dispersal is a passive
process resulting in their random deposition through-
out the environment. Mites deposited on a plant can
probably choose to stay or leave, depending on its
suitability as a host, but it is believed that dispersal-
related mortality is high (Jeppson et al. 1975, Sabelis
1
Current address: Alson H. Smith, Jr., Agricultural Research and
Extension Center, Virginia Polytechnic Institute and State University,
595 Laurel Grove Road, Winchester, VA 22602.
and Bruin 1996). In Florida, the citrus rust mite is
regularly exposed to extreme climatic conditions that
may increase the risks associated with dispersal, rel-
ative to those for species of eriophyids living in tem-
perate climates. Daily maximum temperatures from
June through September often reach levels that are
lethal (Reed et al. 1964) or exceed the limits for re-
production and development (Allen et al. 1995), and
frequent late afternoon or evening storms bring heavy
precipitation and high wind. Heavy dew that fre-
quently develops during the night often does not dry
until midmorning, and the combination of dew and
rainfall frequently results in citrus fruit and foliage
remaining wet for extended periods. Being only ⬇150
␮m long (Jeppson et al. 1975), adult citrus rust mites
are physically constrained from dispersing from wet
fruit and foliage.
Although P. oleivora is one of the most economically
important pests of citrus, little is known about its
population dynamics. Given the fundamental impor-
tance of immigration and emigration to the structure
and development of arthropod populations, the over-
riding objective of the study reported here was to
improve our understanding of how aerial dispersal
may inßuence the population dynamics and manage-
ment of citrus rust mite. SpeciÞc objectives of labo-
ratory and Þeld experiments spanning 3 yr were to
determine the following: (1) the effect of abiotic,
environmental factors on the temporal pattern of dis-
persal and the survival of dispersing mites; (2) the

0046-225X/01/0318Ð0326$02.00/0 䉷 2001 Entomological Society of America

April 2001 BERGH: ECOLOGY AND AEROBIOLOGY OF DISPERSING CITRUS RUST MITES
relationship between population density and dispers-
al; (3) the dispersal distance in commercial citrus
groves; (4) the sex-ratio of dispersing mites; and (5)
the potential for dispersing females to initiate new
populations through oedipal and sibmating.
Materials and Methods
Traps. Three types of traps were used to capture
dispersing mites: unidirectional, omnidirectional, and
Þlter paper.
The unidirectional trap was a 2.5 by 7.6-cm glass
microscope slide with silicone grease (Dow Corning,
Midland, MI) applied thinly to 5.1 cm along the length
of one side. The slide was inserted into a vertical slit
cut in a 1.5-cm i.d. (0.6-inch) conduit pipe coupling
attached to a 1.5-m section of conduit pipe, and held
in place by the second screw on the coupling. The
conduit pipe was inserted vertically into the soil so
that the trapping surface was at ⬇1.2 m elevation. The
unidirectional trap was designed to capture airborne
mites coming only from the direction the trap was
facing. Captured mites were counted using a dissect-
ing microscope at 16 Ð25⫻.
The omnidirectional trap was designed to capture
airborne mites regardless of wind direction, and it was
placed in row middles within a grove. The trap con-
sisted of a 1.5-m length of 1.5-cm i.d. conduit pipe with
a threaded adapter attached to one end. A PVC
adapter was screwed to the conduit pipe adapter and
a 0.3-m section of 2.2-cm o.d. PVC pipe (seven-eighths
in) inserted into the unthreaded end of the PVC
adapter. The trapping surface was a thin layer of sil-
icone grease applied in a 1.5 cm wide band along the
length of one side of a 7 cm long by 2.5-cm wide strip
of clear transparency Þlm (Apollo W0100C, Apollo
Presentation Products, Ronkonkoma, NY). The strip
was wrapped around the PVC pipe, 8.0 cm from one
end, and held in place using double-sided tape at-
tached to the pipe. The conduit pipe was inserted
vertically into the ground and the trapping surface was
at an elevation of ⬇1.7 m. After trapping, the strip was
laid ßat on a 10 by 3.8-cm piece of clear glass (0.25 cm
thick) using double-sided tape, and mites were
counted as described above.
The Þlter paper trap was designed to capture mites
dispersing from individual fruit growing singly in the
outer canopy and hanging vertically at 0.75Ð1.25 m
above the ground. Other fruit near the fruit selected
were pruned, but foliage was pruned minimally. The
trapping surface was a 7-cm-diameter Þlter paper cir-
cle (Whatman No. 50, Whatman International, Maid-
stone, England) marked with a grid pattern, sitting on
wet cotton in a petri dish (19 cm diameter). A
screened cage (1.5-mm2 mesh) with an 18 by 18-cm
wood bottom was screwed to an adapter on a 60 cm
long section of conduit pipe (1.8 cm o.d.; 0.71 inch),
which inserted into an 80 cm long section of pipe (1.9
cm i.d.; 0.75 inch). After the thicker section of pipe had
been placed in the ground below a fruit, an adjustable
collar around the thinner pipe allowed the cage bot-
tom to be positioned ⬇5 cm below a fruit suspended
319
within the cage. Fruit were prevented from swaying
within the cage, using string to secure the branch to
the tops of opposite corner posts. A sliding wooden
sleeve around the bottom of the cage allowed the petri
dish to be centered below the fruit and replaced with-
out touching or moving the fruit.
After trapping, the Þlter paper circles were partially
dried and live mites were counted using backlighting.
Because hundreds of mites were often captured by
these traps, counts were by made placing a black ink
dot on each mite.
Temporal Distribution. To examine the temporal
distribution of aerial dispersal, four omnidirectional
traps were deployed in two ÔValenciaÕ orange groves
near Lake Alfred, FL (Citrus Research and Education
Center (CREC) and Berry), for seven nonconsecu-
tive days in September and October 1997. Beginning
at 0700 hours, the traps were replaced at 2-h intervals
until 1900 hours and then again at 0700 hours the
following day. Preliminary studies in 1996 had shown
that very few mites were trapped between 1900 and
0700 hours. Live mites captured were counted imme-
diately after trap replacement. This test was repeated
in September 1999 using Þve Þlter paper and Þve
omnidirectional traps in a Valencia orange grove at
the CREC for four consecutive days. Omnidirectional
traps were replaced at the same intervals as in 1997.
Filter paper traps were adversely affected by rain and
therefore were not deployed from 1900 to 0700 hours.
Data from each site in 1997 and each trap-type in
1999 were analyzed separately, using PROC analysis of
variance (ANOVA) of SAS (SAS Institute 1988) and
the least signiÞcant difference (LSD) test to compare
the number of mites captured among trapping inter-
vals. All statistical comparisons of data from this and
subsequent tests were made at the 5% level.
Data recorded hourly by the CREC weather station
were used in a stepwise regression (SAS Institute
1988) to determine which of the following variables
best described the dispersal pattern in 1997 and 1999;
time of day, solar radiation (Mjcm-2 in 1997, W/m2 in
1999), temperature (⬚C), relative humidity (%), wind
speed (kph), rain (cm), and leaf wetness (% of leaf
surface). Different instrumentation used in 1997 and
1999 measured solar radiation differently, precluding
an analysis of pooled data.
Survival of Mites Off the Host. The survival of mites
off the host under constant and ambient conditions
was examined. A cohort of adult mites was reared from
late-stage nymphs transferred from Þeld-collected to
clean fruit late in the afternoon. These fruit were held
under humid conditions in a controlled environment
chamber set at 25⬚C and a photoperiod of 14:10 (L:D)
h. At 0630 hours on the morning of the second day
thereafter, 45 adults were placed individually in the
depression on “hanging drop” microscope slides and
conÞned there by a square piece of Þne mesh, nylon
screen glued to the slide using ElmerÕs School glue
(ElmerÕs Products, Columbus, OH). At 0700 hours,
slides with mites were placed on plastic trays, with the
screen facing upward, and held in partially covered,
clear plastic boxes lined with wet paper towel in con-
320 ENVIRONMENTAL ENTOMOLOGY
trolled-environment chambers set at 25, 30, and 35⬚C
(15 mites per temperature). Beginning at 0800 hours,
mortality was assessed at 1-h intervals until all mites
had died, using a dissecting microscope at 10 Ð16⫻.
Dead mites had a contracted body with legs curled
underneath the prodorsal shield. This test was re-
peated twice in late August 1999. One-way ANOVA
followed by the Tukey test were used to compare the
longevity of mites among temperatures.
To determine the effect of time of removal from the
host on the mortality of mites exposed to ambient
conditions outdoors, a cohort of adult mites was gen-
erated as described previously. At 2-h intervals from
0700 to 1300 hours, groups of 15 mites were removed
from fruit and placed individually in depression slide
cages. The slides were placed on plastic trays, with the
screened side facing up, and the trays were placed
under a cardboard canopy on a wooden table exposed
to full sunlight. Beginning 1 h after removal from the
host, mortality was assessed at 1-h intervals until all
mites had died. Ambient temperature and humidity
data were provided by the CREC weather station,
located ⬇75 m from where the test was performed.
This experiment was repeated twice in early Septem-
ber 1999. One-way ANOVA followed by the Tukey
test were used to compare the longevity of mites
removed from the host at different times.
Population Density. Mite population density on 10
fruit was measured in the afternoon in an unsprayed
Valencia orange grove at the CREC. Using a 16⫻
hand-lens, the Rogers et al. (1994) modiÞcation of the
Horsfall-Barratt system (Horsfall and Barratt 1945)
was used to determine the number of mites in four lens
Þelds around the circumference of each fruit. This
method involves assigning the mites to one of seven
size classes (0, 1Ð3, 4 Ð 6, 7Ð12, 13Ð25, 26 Ð50, and ⬎50)
without counting the actual number of individuals.
After density measurements were taken, the fruit
were suspended with the screened cage of the Þlter
paper trap. The traps were deployed the following day
from 0800 to 1200 hours, and captured mites were
counted. Ten new fruit were used each day for Þve
nonconsecutive days in August 1999.
Least-squares linear regression on pooled data were
used to describe the relationship between mite den-
sity and the number of mites captured.
Sex Ratio. Mites were captured in omnidirectional
and Þlter paper traps and sampled from fruit using a
small camelÕs-hair brush on Þve nonconsecutive days
in September and October 1999. Samples were taken
on different days from two groves at the CREC, Lake
Alfred. Five heavily infested fruit were selected in the
afternoon and suspended within the screened cage of
the Þlter paper traps. At 0800 hours the following
morning, a trap was placed in each cage and Þve
omnidirectional traps were also deployed in the row
middles within the grove. Traps were retrieved at 1200
hours. At 1000 hours on each day that traps were
deployed, mites from Þve heavily infested fruit from
the same grove were brushed onto the greased surface
of microscope slides.
Vol. 30, no. 2
The mites captured in each omnidirectional trap
were concentrated in small spots of grease on a glass
slide for storage. A subsample of ⬇30 live, adult mites
from each Þlter paper trap and ⬇50 adults from each
fruit was similarly collected and stored. The species
and gender was determined for all of the mites cap-
tured in omnidirectional traps and for groups of 25
from the subsamples taken from Þlter paper traps and
fruit. Mites were Þrst degreased and Þxed in Hemo-De
(Fisher, Pittsburgh, PA), then cleared in NesbittÕs
solution and slide-mounted in groups in a drop of
NesbittÕs solution. A phase contrast microscope was
used for identiÞcation of species and gender. Gender
determinations were based on examination of the gen-
italia (Lindquist 1996).
The proportion of female P. oleivora in each sample
was calculated and transformed by arcsine square-root
before comparisons among samples from each day
using ANOVA and the Tukey test.
Dispersal Distance. The aerial movement of mites
between adjacent citrus groves was examined at three
locations near Davenport, FL, in September and Oc-
tober 1997. This experiment used the east/southeast
wind that prevails in Florida during the summer and
the fact that unidirectional traps capture only mites
being carried from one direction. At each location,
two commercial citrus groves with north-south ori-
ented rows were separated by a Þeld or a secondary
road. The east grove at each site supported a heavy
population of P. oleivora and was considered the
source of dispersing mites. The adjacent grove, west of
each source grove, was considered the sink for dis-
persing mites.
At the Highway 547 (H547) and Minute Maid Road
(MMR) sites, a Þeld separated ÔHamlinÕ orange groves
by 98 and 103 m, respectively. Four unidirectional
traps were deployed ⬇3 m from the edge of the source
grove, spaced ⬇12 m apart, with trapping surfaces
facing east. Lines of four east-facing traps were also
deployed approximately half-way between the two
groves and at ⬇2 m from the edge of the sink groves.
At the Orchid Drive site, a road separated Valencia
orange groves by 13 m. Only two lines of four traps
(12 m apart) were deployed at Orchard Drive, one at
⬇2.4 m from the source grove and the other at ⬇1.2 m
from the sink grove.
Traps were deployed for three consecutive 7-d in-
tervals at H547 and MMR, and for two consecutive 7-d
periods at Orchard Drive. Traps were replaced after
each 7-d interval and the number of mites captured in
each trap was recorded. Comparisons of trap-catches
among distances from the source grove at each site
used one-way ANOVA followed by the Tukey test
(SAS Institute 1988). Linear regression with a re-
peated measures function was used to predict the log
number of mites trapped as a function of distance.
Nonrandom Mating. The potential for the develop-
ment of local populations based on oedipal mating and
sibmating was examined by generating cohorts of in-
seminated and virgin females. Unsprayed Valencia or-
anges were collected from the Þeld in early June,
washed in distilled water, dried, and dipped in liquid
April 2001 BERGH: ECOLOGY AND AEROBIOLOGY OF DISPERSING CITRUS RUST MITES
Table 1. Mean ⴞ SD number of citrus rust mites captured in dispersal traps deployed in citrus groves near Lake Alfred, FL, in 1997
and 1999
Grove
7Ð9 9 Ð11
CREC (omnidirectional) 0.71 ⫾ 1.1ab 4.0 ⫾ 2.5c
Berry (omnidirectional) 1.0 ⫾ 1.0a 15.7 ⫾ 8.8c
CREC (omnidirectional) 1.0 ⫾ 0.8a 6.0 ⫾ 4.7b
CREC (Þlter paper) 27.8 ⫾ 5.2ab 266.3 ⫾ 153.0c
Four omnidirectional traps per site for 7 d in September and October 1997 at the CREC and Berry groves, respectively. Five omnidirectional
and Þlter paper traps at the CREC for 4 d in September and October 1999. Means within rows followed by the same letter are not signiÞcantly
different at the 5% probability level by ANOVA and the LSD test.
parafÞn wax, leaving about one-third of the surface
unwaxed. The circular, unwaxed area was divided into
four cells using Tangletrap (Tanglefoot, Grand Rapids,
MI), and a single nymph, about to enter the imago-
chrysalis stage (Sternlicht and Goldenberg 1971), was
transferred from Þeld-collected fruit to each cell. The
fruit were held for 2 d under humid conditions in a
controlled-environment chamber at 25⬚C. Citrus rust
mite reproduction is arrhenotokous (Swirski and Ami-
tai 1959), and virgin females that had developed from
isolated nymphs were identiÞed by their deposition of
male eggs within the cell.
Inseminated females were generated by placing vir-
gins on the unwaxed area of fruit on which numerous
males (generated previously by virgin females) had
deposited spermatophores (OldÞeld et al. 1970) dur-
ing the previous 24 h. To maximize the probability of
insemination, virgin females were transferred to areas
with many spermatophores and left on the fruit for 4 h
(OldÞeld and Newell 1973).
Forty unsprayed Valencia fruit were washed and
waxed as described above, leaving a 3.5-cm-diameter
circular area unwaxed. A dissecting microscope was
used to check for extraneous citrus rust mites, their
eggs, or other arthropods in the unwaxed area. Using
a Þne-tipped, indelible ink marker and a template, four
0.5-cm2 observation areas were marked at approxi-
mately equidistant locations around the perimeter of
the unwaxed area. A single inseminated or virgin fe-
male mite was placed in the center of the unwaxed
area on fruit (n ⫽ 20 per group). The fruit were placed
in covered, plastic boxes in a controlled environment
chamber set at 25⬚C and a photoperiod of 14:10 (L:D)
h. High humidity was maintained in the boxes by lining
the bottom with wet paper towel.
After 7 d, the entire unwaxed area on each fruit was
examined for the presence of the female mite and any
of her progeny. During this examination, several adults
were found in the unwaxed area on Þve fruit (two with
inseminated and three with virgin females). The ex-
traneous adults were assumed to have developed from
citrus rust mite eggs overlooked during the inspection
on the Þrst day of the test, and those fruit were dis-
carded. At 7, 21, and 28 d after the onset of the test, the
number of eggs, juveniles, and adult mites inside the
four observation areas on the remaining fruit was
recorded.
321
Trapping interval (time of day)
11Ð13 13Ð15 15Ð17 17Ð19 19 Ð7
1997
2.1 ⫾ 1.1b 1.9 ⫾ 1.3ab 1.3 ⫾ 0.9ab 0.6 ⫾ 0.9a 0.6 ⫾ 0.8a
14.4 ⫾ 5.3bc 12.7 ⫾ 7.1bc 9.0 ⫾ 6.5b 2.7 ⫾ 1.8a 1.4 ⫾ 1.7a
1999
4.0 ⫾ 1.6bc 1.3 ⫾ 1.0ac 1.0 ⫾ 1.2a 0.8 ⫾ 1.0a 0.5 ⫾ 0.6a
124.5 ⫾ 51.8b 58.8 ⫾ 32.5ab 40.3 ⫾ 40.6ab 11.0 ⫾ 11.0a NA
The chi-square test with Yates correction for con-
tinuity was used to compare the number of insemi-
nated and virgin females that had initiated a popula-
tion on fruit by day 28. The criterion used for
population initiation was the presence of more than
Þve individuals from all life stages counted within the
four, 0.5-cm2 observation areas on day 28. One-way
ANOVA followed by the Tukey test were used to
compare the mean number of eggs, juveniles, and
adults found in the observation areas after 28 d.
Results
Temporal Distribution. The capture of dispersing
mites by omnidirectional traps in the Berry and CREC
groves in 1997 showed a diel periodicity. The onset of
dispersal was pronounced, beginning after 0900 hours
(Table 1). Mite captures were statistically largest be-
tween 0900 and 1100 hours at the CREC, and numer-
ically, though not statistically, largest during the same
interval at the Berry grove. In 1997, 75.8 and 71.8% of
the total catch occurred between 0900 and 1500 hours
at the Berry and CREC groves, respectively, and very
few mites were captured after 1700 hours.
The same diel dispersal patterns were recorded at
the CREC grove in 1999 and were independent of the
type of trap or sample size (n ⫽ 2,116 and 59 mites in
Þlter paper and omnidirectional traps, respectively)
(Table 1). The dispersal peak between 0900 and 1100
hours was signiÞcantly different from other trapping
intervals in the Þlter paper traps, and numerically
largest in the omnidirectional traps. The majority of
mites were captured during the 6-h period from 0900
to 1500 hours (84.9 and 76.3% in Þlter paper and
omnidirectional traps, respectively).
The effect of abiotic variables on the capture of
dispersing mites was generally consistent among the
four data sets (Table 2). Solar radiation was the best
one-variable model in all cases. The relationship was
improved considerably by a two-variable model in-
corporating time and leaf wetness for three data sets,
and solar radiation and humidity for one data set. None
of the other variables made important improvements
to the models.
Survival of Mites Off the Host. The longevity of a
cohort of adult mites off the host plant was inversely
related to the constant temperature to which they
322 ENVIRONMENTAL ENTOMOLOGY Vol. 30, no. 2

Table 2. Results of stepwise regression describing the effect of abiotic factors on the capture of dispersing citrus rust mites in traps
replaced at intervals throughout the day

One-variable model Two-variable model

Month/
Grove/trap Parameter Model Parameter Model
year (SE) F P (SE) F P
estimate r2 estimate r2
CREC/omni 9/97 Intercept 0.64 (0.36) 0.186 10.74 ⬍0.01 Intercept 5.43 (0.82) 0.364 13.18 ⬍0.001
Solar radiation 0.66 (0.20) Time ⫺0.25 (0.06)
Leaf wetness ⫺2.65 (0.63)
Berry/omni 10/97 Intercept 1.40 (1.40) 0.437 36.52 ⬍0.001 Intercept ⫺11.40 (5.29) 0.505 23.43 ⬍0.001
Solar radiation 4.28 (0.71) Solar radiation 5.73 (0.89)
Humidity 0.16 (0.06)
CREC/omni 9Ð10/99 Intercept 0.26 (0.66) 0.327 12.65 ⬍0.01 Intercept 12.92 (2.63) 0.441 9.86 ⬍0.001
Solar radiation 0.006 (0.002) Time ⫺0.68 (0.17)
Leaf wetness ⫺0.75 (0.17)
CREC/Þlter 9Ð10/99 Intercept ⫺2.11 (31.92) 0.350 11.85 ⬍0.01 Intercept 586.79 (99.11) 0.559 13.33 ⬍0.001
paper Solar radiation 0.24 (0.07) Time ⫺32.08 (6.40)
Leaf wetness ⫺28.39 (6.39)

No three-variable model signiÞcantly improved the correlation coefÞcient, according to the maximum r2 improvement procedure.

were exposed (Table 3). Adult mites removed from
the host at 2-h intervals between 0700 and 1300 hours
and exposed to ambient temperature and humidity
showed an inverse relationship between longevity and
time of removal (Table 4).
Population Density. There was a signiÞcant, linear
relationship between population density and the num-
ber of mites captured (Fig. 1). Mites were captured
even when populations on fruit averaged less than one
per lens Þeld and ⬎300 mites were captured from
some fruit during the 4-h trapping interval.
Sex Ratio. With exceptions in two traps, the mites
sampled from Þlter paper and omnidirectional traps
were adult females (Table 5). The percentage of fe-
male mites in samples from Þlter paper and omnidi-
rectional traps was signiÞcantly greater than from
samples of mites brushed from fruit in all but one
comparison. The percentage of adult male mites in
samples brushed from individual fruit ranged from 0 to
52% (mean ⫾ SD ⫽ 16.8 ⫾ 13.5%).
Dispersal Distance. At H547 and MMR, more mites
were captured next to the upwind, source grove than
in traps halfway between the groves or next to the
downwind grove; whereas at Orchard Drive, the num-
ber of mites trapped next to the source and sink groves
was not different (Fig. 2). The estimated percentages
and 95% conÞdence intervals of mites that left the
source grove and arrived at the sink grove was 22% (1,
Table 3. Mean ⴞ SD longevity (hours) of a cohort of adult
citrus rust mites removed from fruit and exposed to constant
temperatures
Temp, ⬚C
25 30 35
(n ⫽ 12) (n ⫽ 15) (n ⫽ 15)
27 Aug 1999 14.7 ⫾ 1.2a 9.2 ⫾ 1.4b 4.7 ⫾ 0.9c
30 Aug 1999 14.5 ⫾ 1.3a 10.3 ⫾ 2.8b 5.7 ⫾ 1.0c
Means within rows followed by the same letter are not signiÞcantly
different at the 5% probability level by ANOVA and the Tukey test.
Sample sizes vary as a result of a few mites being discarded because
of being stuck in the glue or escaping from the cage.
35), 13% (0.3, 20), and 150% (73, 307) for the H547,
MMR, and Orchard Drive sites, respectively.
Nonrandom Mating. Based on the criterion used,
equal numbers of inseminated (n ⫽ 13) and virgin
(n ⫽ 12) females initiated populations (␹20.05, 1 ⫽
1.261, P ⬎ 0.25). The mean (⫾SD) number of eggs,
juveniles, and adults counted in the observation areas
after 28 d was the same whether they were produced
by virgin or inseminated females: eggsÐinseminated ⫽
29.3 ⫾ 44.9; virgin ⫽ 12.3 ⫾ 7.5; F ⫽ 1.68; df ⫽ 1, 23;
P ⫽ 0.2078; juvenilesÐinseminated ⫽ 10.6 ⫾ 16.1; vir-
gin ⫽ 5.2 ⫾ 3.3; F ⫽ 1.31; df ⫽ 1, 23; P ⫽ 0.2633;
adultsÐinseminated ⫽ 10.1 ⫾ 14.0; virgin ⫽ 3.3 ⫾ 2.2;
F ⫽ 2.70, df ⫽ 1, 23; P ⫽ 0.1140.
Discussion
The dispersal behavior of the citrus rust mite ap-
pears to be shaped by a combination of abiotic factors.
The onset of dispersal each day is probably triggered
by the drying of dew. Mites submerged in rain or dew
are physically prevented from dispersing by the wa-
terÕs surface tension. This effect may account for the
consistent contributions of solar radiation and time
and leaf wetness to the one- and two-variable models
describing the relationship between abiotic factors
and the dispersal pattern, and may partially explain the
lack of dispersal at night. Peak dispersal activity occurs
from late morning until early afternoon, declining
thereafter to relatively low levels during the remain-
ing daylight hours.
In contrast to the results reported here, the aerial
dispersal of other eriophyid species was correlated
with wind velocity alone (Staples and Allington 1956)
or a combination of temperature and wind velocity
(Nault and Styer 1969). These variables had negligible
impact on the dispersal model developed for citrus
rust mite, probably due to the different species of
mites studied and to the different sampling regimes.
Whereas the current study used 2-h sample intervals
throughout most of the day and 12-h intervals over-
night, Nault and Styer (1969) and Staples and Alling-
April 2001 BERGH: ECOLOGY AND AEROBIOLOGY OF DISPERSING CITRUS RUST MITES 323

Table 4. Longevity of a cohort of adult citrus rust mites removed from the host at intervals and exposed to ambient conditions

Time of removal from fruit

0700 0900 1100 1300
hours hours hours hours
2 Sept 1999 (n ⫽ 15) (n ⫽ 13) (n ⫽ 15) (n ⫽ 14)
Mean ⫾ SD longevity (hours) 7.6 ⫾ 0.5a 5.8 ⫾ 0.4b 4.1 ⫾ 0.3c 3.6 ⫾ 0.9c
Temp, ⬚C 22.8 27.4 30.7 31.6
% RH 99.1 80.4 65.5 56
3 Sept 1999 (n ⫽ 15) (n ⫽ 15) (n ⫽ 14) (n ⫽ 14)
Mean ⫾ SD longevity (hours) 7.3 ⫾ 0.5a 5.1 ⫾ 0.5b 3.7 ⫾ 0.5c 2.6 ⫾ 0.5d
Temp, ⬚C 21.4 27.7 30.8 33.6
% RH 100 63.3 53.3 38.9

Means within rows followed by the same letter are not signiÞcantly different at the 5% probability level by ANOVA and the Tukey test. Sample
sizes vary as a result of a few mites being discarded because of being stuck in the glue or escaping from the cage.

ton (1956) related environmental data to 24-h cap-
tures of Aculodes dubius and Aceria tulipae
(tosichella), respectively. A 24-h sampling regime may
or may not reveal the key environmental factors that
regulate the dispersal of eriophyid mites, especially if
the dispersal of a given species shows a diel period-
icity.
Frost (1997) discussed the conditions that favor the
successful arrival of an aerially dispersing eriophyid
mite at a new host, including the spatial distribution of
hosts and the duration of survival during dispersal, as
inßuenced by the miteÕs buoyancy and ability to avoid
desiccation. Adult grain rust mites, Abaracus hystrix
(Nalepa), increased their production of wax Þlaments
in response to high temperatures (Frost 1997). Com-
pared with unwaxed individuals, waxed mites lived
longer at low humidity and showed reduced terminal
Fig. 1. Least squares linear regression of the relationship
between the population density of citrus rust mites on fruit
and the number of dispersing mites captured in traps. Pa-
rameter estimate ⫾ SE; intercept: 5.30 ⫾ 2.37, trap 11.73 ⫾
1.56, model r2 ⫽ 0.546; F ⫽ 56.58; df ⫽ 1, 47; P ⬍ 0.0001.
velocity in a column of still air, which implies in-
creased buoyancy and potentially greater time aloft.
Citrus rust mites do not show any apparent mor-
phological adaptations that could enhance survival
during dispersal; however, they may maximize their
potential Þtness through adaptive migratory behavior.
Measurements of the mortality of mites removed from
the host suggest that dispersal during a 2- to 3-h period
following the drying of dew should increase survival
by reducing the duration of exposure to the higher
temperatures and lower humidity which characterize
the afternoon hours (Tables 3, 4, and 6).
Based on the environmental conditions character-
istic of the period of peak dispersal in the morning, the
late afternoon and early evening periods would also
appear favorable for the dispersal of mites (Table 6).
The lack of dispersal from late afternoon onward may
be an adaptive response to the brief, but intense rain-
fall that frequently occurs in the interior of central
Florida during the summer months. These storms
rarely occur before ⬇1400 hours, but are common in
the late afternoon and evening. Citrus rust mites can
attach themselves Þrmly to the host plant using their
caudal lobes, and are probably not washed off by
heavy rain. Whether this attachment behavior occurs
in response to changing barometric pressure or hu-
midity associated with the onset of these storms is
unknown. J.C.B. (unpublished data) has found that
citrus rust mites transferred to a wet surface cease
moving immediately and do not struggle or attempt to
walk. This behavioral response to wetting may be an
adaptation that conserves energy during regular pe-
riods of immersion in rain and dew.
The aerial dispersal of citrus rust mites from fruit
was independent of population density; mites were
captured from 49 of 50 fruit sampled, even though the
density of mites on nine fruit averaged less than two
per lens Þeld. Bergh and McCoy (1997) captured
dispersing mites very early in the season, when pop-
ulations on fruit were nearly undetectable. These re-
sults concur with those of previous studies showing
that aerial dispersal of eriophyid mites occurs through-
out the season and seems to be independent of pop-
ulation density or host plant quality (Sabelis and Bruin
1996). Lawson et al. (1996) reported similar observa-
tions for the European red mite, Panonychus ulmi
324 ENVIRONMENTAL ENTOMOLOGY
Table 5. Mean ⴞ SD percentage of female citrus rust mites in samples of mites brushed from fruit and captured while dispersing
Date Brushed from fruit
(1999) Na % female
17/9 125 67.2 ⫾ 18.0a
28/9 125 81.6 ⫾ 12.8a
30/9 125 95.2 ⫾ 3.3a
7/10 125 88.0 ⫾ 6.3a
12/10 124 83.9 ⫾ 4.8a
Means within rows followed by the same letter are not signiÞcantly different at the 5% probability level based on ANOVA and Tukey test
analyses on arcsine transformed percentages.
a
Total number of Phyllocoptruta oleivora in subsamples of 25 mites taken from Þve fruit and Þve Þlter paper traps per day. Sample size from
omnidirectional traps represent the total number of P. oleivora captured by Þve traps each day.
(Koch), and speculated that a density-independent
proportion of mites is committed to disperse. Sabelis
and Bruin (1996) made the same tentative interpre-
tation from data on vagrant species of eriophyids. The
dispersal behavior of citrus rust mite is gender-spe-
ciÞc, concurring with KrantzÕs (1973) observations on
the rust mite Aculus cornutus (Nalepa). The underly-
ing mechanisms that trigger dispersal in some propor-
tion of females in every population remain unknown.
Gender-speciÞc dispersal may have contributed to
some of the variability not explained by the model
describing the relationship between population den-
sity on fruit and the number of mites captured in traps.
Because the Þlter paper traps capture mites leaving a
single fruit, the sex ratio of mites on a fruit would
inßuence the proportion of the population available
for trapping. On each of 2 d, a single fruit with a high
mite population yielded very few dispersers. The per-
centage of males in samples brushed from individual
fruit with high populations varied from 0 to 52%, and
Swirski and Amitai (1960) reported that the percent-
age of male citrus rust mite on leaves and fruit in late
summer in Israel could exceed 80%. It is impossible to
distinguish male and female citrus rust mites without
examining the genitalia, and this lack of information on
the sex ratio on fruit from which dispersing mites were
trapped may have introduced some variability into the
model.
The Þtness of dispersing female citrus rust mites
depends ultimately on their arrival at suitable host
plants and their contribution to or initiation of a pop-
ulation. Relative to eriophyid species colonizing hosts
that are patchy in distribution, citrus rust mites in
Florida may have a higher probability of arriving at a
new host because of citrus monoculture over large and
contiguous areas. However, dispersal-related mortal-
ity is probably high and may be partially affected by
within-tree rust mite distributions. Allen and McCoy
(1979) found high rust mite populations in the north-
and south-bottom quadrants of trees, where temper-
atures were favorable for development, and the lowest
mite densities in the south-top quadrant, where lethal
temperatures were recorded.
Given this distribution pattern, research on the aer-
ial dissemination of fungal spores from a plant canopy
may help our understanding of the dispersal success of
citrus rust mite. Aylor (1990) reviewed the dissemi-
nation of fungal pathogens by wind. The majority of
Vol. 30, no. 2
Filter paper traps Omnidirectional traps
n % female n % female
125 100 ⫾ 0b 5 100 ⫾ 0b
125 100 ⫾ 0b 7 100 ⫾ 0b
125 100 ⫾ 0b 3 100 ⫾ 0b
111 100 ⫾ 0b 26 88.6 ⫾ 18.6ab
115 98.2 ⫾ 2.5b 20 100 ⫾ 0b
fungal spores are often produced in the lower portions
of the plant canopy because of favorable conditions
there. Lower wind-speed and less turbulence in the
lower canopy limit the escape of those spores except
during a period around midday, when wind-speed and
turbulence near the ground are usually highest. Gra-
dients of disease severity typically decrease rapidly
with increasing distance from the source of spores. As
suggested by the distribution of citrus rust mites
within a tree, the majority of dispersal is from lower
portions of the canopy. A potential consequence of
this is a shorter distance traveled, relative to mites that
leave from higher in the canopy, and a large percent-
age of dispersing mites settling out of the air onto
nonhost plants. This settling of dispersing mites should
be examined using ßat traps positioned horizontally at
ground level with the trapping surface facing upward.
One aspect of the aerial dispersal of citrus rust mite
that has received only cursory attention is the long-
distance transport of mites. In previous studies (J.C.B.,
unpublished data), sticky traps were deployed at an
elevation of ⬇25 m by attaching them to the frame of
two Þre towers in central Florida for two 2- to 3-wk
periods in July and August 1996. Citrus rust mites were
captured in all eight traps on each tower during each
sample period. However, eriophyid mites carried up-
ward from the canopy and transported long distances
would likely suffer extremely high mortality as a func-
tion of prolonged exposure to the elements, and a
greatly reduced probability of being deposited on a
suitable host plant.
Regardless of the mortality that occurs during dis-
persal, these data show that some mites were carried
from a grove to an adjacent grove downwind and that
the percentage of mites arriving at the downwind
location depended on the distance between the
groves. For groves separated only by a secondary road,
which occurs commonly in central Florida, the re-
gression model predicted a greater percentage of
mites arriving at the sink grove than had left the source
grove. Although this prediction is nonsensical and
probably a function of the sampling method, it does
indicate the magnitude of movement possible be-
tween adjacent groves. Bergh and McCoy (1997) dis-
cussed the potential implications of such movement
on mite management programs in central Florida,
where the majority of citrus is grown in adjacent 2- to
9-ha blocks and where pest management practices
April 2001 BERGH: ECOLOGY AND AEROBIOLOGY OF DISPERSING CITRUS RUST MITES 325

Table 6. Representative temperature, humidity and wind

speed data recorded at Lake Alfred, FL, between the 14th and 16th
day of the 4 mo that span the period of peak citrus rust mite
population growth in Florida

0900 Ð1200 1300 Ð1600 1700 Ð2000

Month
hours hours hours
Mean temp (⬚C) and range
June 30.3 (28.1Ð32.8) 32.0 (26.4Ð35.4) 27.1 (23.8Ð33.7)
July 30.8 (28.8Ð33.5) 32.0 (26.9Ð34.9) 26.6 (24.2Ð29.1)
Aug 31.6 (29.4Ð33.6) 34.2 (31.6Ð35.8) 27.9 (22.4Ð32.4)
Sept 28.8 (25.1Ð32.2) 30.6 (28.2Ð33.6) 27.5 (24.5Ð32.9)
Mean relative humidity (%) and range
June 70.5 (57.1Ð86.5) 59.1 (42.5Ð86.6) 81.2 (45.7Ð100)
July 65.7 (50.4Ð81.2) 57.8 (45.7Ð76.8) 85.1 (72.3Ð98.5)
Aug 71.6 (60.2Ð84.5) 56.5 (49.4Ð69.8) 81.0 (59.4Ð100)
Sept 76.9 (59.6Ð90.8) 65.4 (43.7Ð89.3) 76.1 (44.6Ð100)
Mean wind speed (kph) and range
June 5.9 (4.3Ð7.2) 7.1 (2.6Ð18.5) 5.8 (1.1Ð14.8)
July 6.8 (3.9Ð10.6) 9.3 (2.9Ð14.0) 7.9 (3.9Ð10.9)
Aug 5.8 (3.2Ð9.0) 6.3 (3.9Ð9.9) 9.7 (4.7Ð20.1)
Sept 15.6 (4.3Ð25.4) 15.8 (9.0Ð23.0) 10.8 (6.0Ð19.0)

founding of local populations through nonrandom,

Fig. 2. Number of dispersing citrus rust mites captured in
traps deployed between two adjacent citrus groves at three
locations. For each of three 7-d trapping intervals at Minute
Maid Road and Highway 547, bars from left to right are data
from traps next to the source grove, half-way between the
source and sink groves, and next to the sink grove, respec-
tively. For the two trapping intervals at Orchid Drive, left and
right bars are data from traps next to the source and sink
groves, respectively.
may differ widely between groves. Whether the aerial
movement of mites adversely affects the success and
cost of management programs in some situations is not
known, but is worthy of further investigation.
Laboratory tests have shown that a combination of
oedipal mating and sibmating can result in the found-
ing of a local population by a single virgin or insem-
inated female citrus rust mite. It is probable that most
female eriophyids are inseminated before dispersal
(OldÞeld and Newell 1973), in which case sibmating
among F1 progeny would be most relevant to the
initiation of a local population. A dispersing female
mite might also arrive in the midst of an established
population on a new host. Alternatively, when popu-
lations are low early in the season or following a
pesticide application, there could be few or no con-
speciÞcs in her vicinity, and these divergent scenarios
would have very different outcomes with respect to
the genetic structure of the ensuing population. The
sibmating could have important implications for the
development of acaricide resistance in citrus rust mite
populations. Population structure is inßuenced by the
size of breeding units, the number of founding fe-
males, the sex ratio, immigration and emigration, and
nonrandom mating (Roush and Daly 1990). Resis-
tance to dicofol (Omoto et al. 1994) and shifts in
susceptibility to abamectin (Bergh et al. 1999) have
been reported in Þeld populations of citrus rust mite,
and the genetic consequences of these reproductive
strategies for the evolution of resistance in citrus rust
mite populations merit investigation.
The traps used in these studies have proven useful
for addressing questions about the aerial dispersal of
citrus rust mite. Bergh and McCoy (1997) used uni-
directional traps to monitor the dispersal of citrus rust
mite through time and reported strong correlations
between trap-catch and population density on fruit.
They discussed the possibility of using dispersal traps
to monitor mite populations for management pur-
poses. This objective was pursued over several years
by examining the effects of grove location and age,
fruit variety, trap placement, sample interval, and trap
type (i.e., unidirectional and omnidirectional) on the
relationship between trap-catch and population den-
sity. Although some data sets yielded strong correla-
tion coefÞcients, the variability among locations and
years was great and was not consistently improved by
any approach (J.C.B., unpublished data). Although
the traps are useful research tools, they are not suit-
able for use in a monitoring program upon which pest
management decisions are based.
Further research on the biology of dispersing citrus
rust mites could use the advantages associated with
the Þlter paper trap. Whereas unidirectional and om-
nidirectional traps kill the mites they capture and yield
relatively small samples, the Þlter paper trap can pro-
vide large numbers of live mites that could be used to
address questions about population dynamics and
326 ENVIRONMENTAL ENTOMOLOGY
management. For example, comparing the fecundity
and longevity of dispersing females with females of
known age would establish the age at which females
disperse and their potential reproductive capacity.
Bergh and McCoy (1997) also captured dispersing
citrus rust mites infected with the entomopathogenic
fungus, Hirsutella thompsonii. Filter paper traps could
be deployed under fruit on which a fungal epizootic
was occurring; and by culturing captured mites on
media, the effect of a fungal epizootic on the dispersal
behavior of populations and individuals could be mea-
sured.
Acknowledgments
Thanks to J. Waldow, T. Wilkinson, S. Blackburn, and S.
Sloan for technical assistance; J. Harrison and J. Fan for
statistical help; R. Kerr and Holly Hill Groves for their gen-
erous cooperation; and the Florida Citrus Production Re-
search Advisory Council for partial Þnancial support. The
general assistance of the faculty and staff at the Lake Alfred
Citrus Research and Education Center over the past 5 yr is
greatly appreciated. Florida Agricultural Experiment Station
Journal Series No. R07577.
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Received for publication 28 April 2000; accepted 16 Novem-
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