Establishment of Aphytis holoxanthus as a parasite of Florida red scale in Florida


Clancy, D.W.; Selhime, A.G.; Muma, M.H.

Journal of Economic Entomology 56(5): 603-605

1963


In the fall of 1960 Aphytis holoxanthus DeBach, a parasite of the Florida red scale (Chrysomphalus aonidum (L.) in Hong Kong and Israel, was introduced into eight orange groves in central Florida. The parasite soon became established and in 1 year had dispersed to most of the citrus-growing areas of the State. Rapid establishment, increase, and natural spread indicate that this parasite is well adapted to Florida conditions and may become an important factor in the biological control of Florida red scale. The parasite has also been recovered from C. aonidum on plant hosts other than citrus.

October
1963
JOHNSON:
HELICOPTER
APPLICATION
OF
GurrinoN
603
Johnson,
Norman
E.
1962.
Tests
of
Guthion
for
the
control
of
the
Douglas-fir
cone
midge.
Jour.
Econ.
Ent.
55(5):
613--6.
Merkel,
E.
P.,
W.
L.
Beers,
and
P.
E.
Hockston.
1959.Prob-
lerns
involved
in
the
control
of
cone
insects
by
aerial
spraying.
Proc.
Fourth
South.
Conf.
on
Forest
Tree
Improvement,
pp.
77-88.
Merkel,
E.
P.,
and
B.
H.
Ebel.
1961.
Cone
and
seed
insects
and
their
control.
Proc.
Sixth
South.
Conf.
on
Forest
Tree
Improvement,
pp.
137-41.
Steinbrenner,
E.
C.,
J.
W.
Duffield,
and
R.
K.
Campbell.
1960.
Increased
cone
production
of
young
Douglas-fir
following
nitrogen
and
phosphorus
fertilization.
Jour.
Forestry
58(2):
105-10.
Establishment
of
Aphytis
holoxanthus
as
a
Parasite
of
Florida
Red
Scale
in
Florida'
1).
w.
CLANCY,
2
ALLEN
G.
SELIIIME,
3
and
MARTIN
H.
MUMA
4
ABSTRACT
In
the
fall
of
1960
Aphytis
holoranthus
DeBach,
a
parasite
of
the
Florida
red
scale
(Chrysomphalus
aoniduni
(L.))
in
Hong
Kong
and
Israel,
was
introduced
into
eight
orange
groves
in
cen-
tral
Florida.
The
parasite
soon
became
established
and
in
1
year
had
dispersed
to
most
of
the
citrus-growing
areas
of
the
State.
Rapid
establishment,
increase,
and
natural
spread
indicate
that
this
parasite
is
well
adapted
to
Florida
conditions
and
may
become
an
important
factor
in
the
biological
control
of
Florida
red
scale.
The
parasite
has
also
been
recovered
from
C.
aonidunt
on
plant
hosts
other
than
citrus.
Of
the
many
species
of
scale
insects
found
in
Florida
citrus
groves,
Florida
red
scale
(Chrysomphalus
aonidum
(L))
is
second
only
to
purple
scale
(Lepidosaphes
beelcii
(Newman))
in
economic
importance.
Heavy
infestations
of
Florida
red
scale
can
develop
at
any
time,
but
popula-
tions
are
usually
highest
in
fall
and
winter
with
winter
in-
festations
more
damaging
(Muma
1959).
The
Florida
red
scale
can
cause
severe
defoliation
and
fruit
drop.
Although
Muma
(1959)
has
reported
that
Florida
red
scale
is
usually
under
adequate
natural
control
except
where
chemical
applications
or
adverse
weather
condi-
tions
have
upset
the
natural
balance,
it
was
felt
that
bio-
logical
control
of
this
scale
could
be
improved.
Until
recently
Florida
red
scale
was
a
severe
pest
of
citrus
in
Israel.
In
1956
colonies
of
an
Aphytis,
then
be-
lieved
to
be
lingnanensis
Compere,
were
imported
into
Israel
from
Hong
Kong
for
trial
against
this
pest,
even
though
lingnaitensis
was
known
to
parasitize
only
the
California
red
scale
(Aonidiella
aurantii
(Alaska)).
These
parasites
rapidly
became
established
and
produced
outstanding
biological
control
of
the
scale
within
2
to
3
years
(DeBach
1960).
Later
study
revealed
that
the
Is-
raeli
introductions
were
a
new
species,
Aphytis
holoxan-
thus
DeBach,
which
long
had
been
confused
with
lingua-
nensis,
and
that
holoxanthus
was
actually
a
specific
parasite
of
Florida
red
scale
(DeBach
1960).
The
recent
widespread
reduction
of
purple
scale
in
Florida by
the
parasite
Aphytis
lepidosaphes
Compere
(Minna
&
Clancy
1961a,
Simanton
1960)
suggested
that
similar
results
might
be
obtained
with
Florida
red
scale
through
the
introduction
of
A.
holoxanthus.
The
results
of
surveys
to
determine
the
extent
of
establishment
and
nat-
ural
spread
of
A.
holoxanthus
since
its
introduction
in
Florida
citrus
groves
in
the
fall
of
1960
are
presented
in
this
paper.
INTRODUCTION
OF
THE
PARASITE.—Ill
1959
a
breeding
stock
of
A.
holoxanthus
was
obtained
from
Israel
by
the
Entomology
Research
Division's
Parasite
Introduction
Laboratory
at
Moorestown,
New
Jersey,
and
cultures
were
sent
to
the
University
of
California
Citrus
Experi-
ment
Station
at
Riverside
for
experimental
study.
Ar-
rangements
were
then
made
by
the
senior
author
to
ob-
tain
this
parasite
from
the
Riverside
Station
for
coloniza-
tion
in
Florida.
Five
shipments
of
adult
parasites
were
received
from
California
between
August
31
and
November
23,
1960,
and
about
15,420
females
were
released
in
seven
Florida
orange
groves
during
the
same
period.
An
eighth
release
occurred
when
a
few
A.
holoxanthus
left
in
the
containers
were
discarded
in
the
Citrus
Experiment
Station
grove.
About
100
female
and
30
male
parasites
per
tree
were
usually
released,
and
most
trees
received
a
second
release
4
to
6
weeks
later.
The
males
in
the
second
release
were
used
to
increase
the
mating
opportunities
of
the
emerging
F'
females.
The
release
groves
were
widely
distributed
in
five
counties,
and
ranged
from
the
Umatilla
area
in
Lake
County
south
to
the
Arcadia
area
of
De
Soto
County
in
central
Florida.
Unsprayed
groves
were
selected
to
avoid
any
detrimental
effects
of
sprays
on
the
parasites,
and
all
groves
were
heavily
infested
with
Florida
red
scale.
SURVEY
TECHNIQUES.—During
the
fall
and
winter
of
1960,
10
scale-infested
leaves
were
collected
from
each
of
the
parasite-release
trees
about
every
6
weeks.
These
samples
were
placed
in
quart-sized
ice-cream
cartons
fitted
with
plastic
funnels
and
test
tubes
to
attract
the
emerging
parasites
to
the
light.
The
samples
were
held
at
80°
F.
until
all
adult
parasites
had
emerged,
when
they
were
removed
and
counted.
In
1961
the
survey
was
extended
to
all
major
citrus-
growing
areas.
Groves
were
examined
at
random
and
if
infestations
were
sufficiently
heavy,
enough
scale-infested
leaves
were
collected
to
provide
at
least
200
adult
female
scales
per
sample.
In
heavy
infestations
at
least
10
leaves
Accepted
for
publication
November
26,
1902.
2
Entomolo
g
y
Research
Division,
U.S.D.A.,
Riverside,
California
(formerly
at
Lake
Alfred,
Florida).
Entomology
Research
Division,
U.S.D.A.,
Lake
Alfred,
Florida.
4
University
of
Florida
Citrus
Experiment
Station,
Lake
Alfred.
Florida.
604
Jou
liNAL
OF
ECONOM
IC
ENTOMOLOGY
Vol.
56,
No.
5
8
R+
UMATILLA
R+
+
*
O
ORLANDO
R
N
+
*+
* *
0
0
+
_i
L
tgEo
0
R+
8
+SARASOTA
FOR
PIERCE
ARCADIA
R R
+
FORT
MYERS
FIG.
1.—Releases
and
recoveries
of
A
phytis
holoxanthus
in
Florida
citrus
groves,
1960-61.11
=
parasite
release
grove,
0=
none
parasitized,
=trace
to
10%
parasitized,
+
=10%
to
30%
parasitized,
*=over
30%
parasitized.
Clear
areas
are
citrus-
producing.
(20
scales
per
leaf)
were
used
to
make
up
a
sample;
in
lighter
infestations
more
leaves
were
examined
but
sam-
ples
sometimes
totaled
less
than
200
scales.
The
leaves
were
examined
under
a
binocular
microscope,
the
adult
female
armors
turned
over,
and
the
scales
recorded
as
liv-
ing,
dead
(unparasitized),
or
parasitized.
The
scales
counted
as
having
been
parasitized
included
those
with
living
parasite
stages
and
those
showing
parasite
emer-
gence
holes.
Parasites
counted
were
A.
holoxanthus,
Pseudhomalopoda
prima
(Girard),
and
a
chytrid
fungus
Mylaphagus
sp.
Florida
red
scale
infestations
on
hosts
other
than
citrus
were
also
examined
for
A.
holoxanthus.
A.
holoxanthus
was
distinguished
from
so-called
Aphytis
chrysomphali
(Afercet),
the
only
other
external
parasite
of
Florida
red
scale
in
Florida,
by
its
attack
of
adult
female
scales
and
by
the
characteristic
dark
pig-
mented
areas
on
the
venter
of
the
pupal
thorax
and
ab-
domen.
A.
chrysomphali
attacks
only
subadult
males
and
second-stage
females,
and
the
pupae
are
entirely
light
lemon
yellow
in
color
(Minna
1959).
By
the
fall
of
1961
holoxanthus
had
spread
to
most
of
the
citrus
areas
and
data
are
now
being
obtained
pri-
marily
from
a
cooperative
armored
scale
parasite
survey
(Mama
&
Clancy
1961b).
In
this
survey
100
leaf
samples
are
collected
at
random
from
4
marked
trees
each
quarter
in
27
groves
extending
from
Marion
to
Highlands
County
in
Central
Florida.
Nine
of
these
groves
are
untreated,
9
are
treated
with
the
recommended
spray
materials
with-
out
sulfur,
and
9
receive
sulfur
in
addition
to
the
usual
spray
schedules.
The
leaves
are
examined
and
parasitism
is
recorded
as
described
above.
REST:MTS.
Although
hurricane
"Donna"
severely
bat-
tered
several
of
the
parasite-release
groves
in
September
1960,
initial
scale
collections
during
the
next
2
months
yielded
numerous
A.
holoxanthus
from
5
of
these
groves.
However,
infestations
decreased
to
very
low
levels
during
the
winter
and
only
a
few
holoxanthus
were
reared
from
similar
collections
in
January
and
February,
1961.
In
the
spring
of
1961,
holoxanthus
was
observed
and
collected
in
most
of
the
colonized
groves
despite
the
con-
tinued
scarcity
of
hosts.
In
April
the
parasite
was
also
recovered
in
the
Orlando
area,
some
14
to
20
miles
from
the
nearest
release.
Random
survey
collections
in
May,
June,
and
July
extended
the
known
distribution
of
holoxanthus
to
the
west-coast
citrus
areas
of
Sarasota
and
Fort
Myers
across
35
miles
of
predominantly
swamp
and
rangeland,
and
for
shorter
distances
in
several
other
parts
of
the
State.
The
distribution
and
relative
abundance
of
holoxanthus
up
to
October
10,
1961
is
shown
in
figure
1.
The
parasite,
recorded
from
48
of
67
scale
collections
during
August
and
September,
was
most
abundant
in
the
north,
central,
and
west-coast
samples
and
least
abundant
in
the
south
and
east-coast
collections.
Lack
of
continuous
citrus
plantings
between
central
Florida
and
the
south
and
east-coast
areas
apparently
retarded
the
natural
spread
of
holoxan-
thus
in
those
directions.
However,
the
parasite
emerged
from
Florida
red
scale
collected
on
Seheffiera
sp.
in
Fort
Pierce
in
September
and
on
Ligustrunt
sp.
in
Miami
in
November,
which
indicated
dispersal
of
some
80
and
140
miles
from
the
nearest
release
grove.
A.
holoxanthus
also
became
more
abundant
in
the
southern
citrus
area
during
the
winter
of
1961-62
and
was
found
in
4
of
6
collections
on
Merritt
Island
and
adjacent
east-coast
groves
in
March,
1962.
As
noted
in
figure
1,
parasitism
was
usually
highest
in
and
near
the
release
groves.
Parasitism
of
adult
female
scales
by
A.
holoxanthus
ranged
from
0
to
84.2%,
with
an
average
of
18.6%;
by
P.
prima,
from
0
to
58.5%,
with
an
average
of
12.6%,
and
by
Alyiophagus
sp.,
from
0
to
12.5%,
with
an
average
of
1.4%.
Average
parasitism
by
the
three
species
combined
was
32.6%.
Three
successive
samples
collected
in
the
same
loca-
tions
from
August
to
November,
1961,
usually
revealed
increased
parasitism
by
holoxanthus
in
the
later
counts
(table
1).
When
initial
parasitism
was
high,
variable
rates
were
obtained
in
later
samples,
an
indication
that
a
bal-
ance
may
already
have
been
reached
in
certain
groves.
A.
holoxanthus
was
also
found
attacking
Florida
red
scale
on
Ligustrum
sp.
in
Orlando
and
Zamia
sp.
in
Winter
Haven
and
Orlando.
The
relative
abundance
of
A.
koloxanthus
and
P.
prima
in
the
27
armored
scale
survey
groves
from
the
fall
of
1960
to
the
summer
of
1962
is
shown
in
table
2.
Although
holoxanthus
did
not
appear
in
these
samples
until
the
spring
of
1961,
it
increased
steadily
in
both
distribution
and
abundance
during
the
year.
Further
increase
in
1962
may
have
been
prevented
by
unusually
low
scale
popula-
tions
in
most
of
these
groves.
In
fact,
this
parasite
may
be
responsible
for
the
steady
decline
of
scale
populations
MERRITT
ISLAND
R+
-
00
0
October
19G.3
CLA
NCY
ET
A
L.
:
APIIYTIS
HOLOXANTHUS
AS
FLORIDA
RED
SCALE
PARASITE
605
Table
1.-Percent
of
Florida
red
scale
parasitized
by
Aphytis
holoxanthus
and
Pseudhomalopoda
prima
in
three
successive
foliage
samples,
1961,
Florida.
SAMPLE
I
SAMPLE
2
SAMPLE
3
SCALE
HOST
AND
LOCATION
A
holox.
P
prima
A
holm
P
prima
A
haw.
prima
Orange,
Lake
Wales
72.8
8.0
45.1
19.8
29.3
3.0
Grapefruit,
Dundee
58.4
2.6
62.4
1.7
38.7
14.5
Grapefruit,
Lake
Alfred
1.1
54.0
51.9
16.9
17.8
29.6
Orange,
Lake
Alfred
0.0
10.5
0.3
21.4
60.8
16.6
Lilustram
sp..
Orlando
9.3
50.5
30.6
51.7
25.5
23.9
Zamia
sp.,
Winter
Ilaven
1.6
34.9
12.8
8.9
49.4
7.1
since
the
fall
of
1961
(table
2).
There
are
also
recent
indi-
cations
that
parasitism
by
P.
prima,
the
critical
native
primary
parasite
of
Florida
red
scale,
has
been
reduced
through
competition
with
holo.raothus
since
both
spe-
cies
attack
the
same
host
stage.
Disct7ssioN.-A.
holoxanthus
rapidly
became
estab-
lished
from
initial
releases
in
central
Florida
and
in
1
year
had
spread
to
most
of
the
citrus-producing
areas
of
the
State.
Parasite
dispersal
may
have
been
assisted
by
high
winds
accompanying
hurricane
"Donna"
which
struck
central
Florida
soon
after
the
first
releases
had
been
made.
Unintentional
establishment
of
holoxanthus
on
the
Citrus
Experiment.
Station
grounds
also
demonstrated
its
ability
to
develop
from
very
small
numbers.
The
parasite
has
survived
2
winters
without
apparent
reduction
and
seems
well
adapted
to
Florida
conditions.
Although
its
relative
abundance
in
sprayed
groves
indi-
cates
a
general
compatibility
with
many
pesticides,
sulfur
may
he
detrimental
as
with
other
scale
parasites
(Muma
&
Clancy
1961b).
Recovery
of
holoxanthus
from
Florida
red
scale
infest-
ing
ornamental
nursery
plants
of
Ligustrion
sp.
and
Schltera
sp.
and
also
from
the
native
Florida
"coonti"
(a
cycad,
Zamia
sp.)
indicates
adaptation
of
the
intro-
duced
parasite
to
a
wide
variety
of
habitats
and
vegeta-
tion.
The
"coonti"
is
a
common
wild
plant
in
south
Florida
and
is
generally
infested
with
red
scale.
These
Table
2.-Abundance
of
Pseudhomalopoda
prima
and
Aphytis
holoxanthus
in
27
Florida
groves
surveyed
for
parasitism
of
Florida
red
scale,
1960-62,
Florida.
NUMBER
OP
LIVING
P.
prima
A.
holoranthus
Number
of
Groves
Percent
Number
of
Groves
Percent
SEASON
AND
UNPAIIABITIZED
Where
Para-
Where
Para-
YEAH
SCALES
Found
sitized
Found
sitized
Fall,
1960
70
22
52.6
0
0
Winter,
1960-61
52
41
37.5
0 0
Spring,
1961
148
11
21.1
1
7.1
Summer,
1961
208
16
12.1
7
14.7
Fall.
1961
41
16
13.8
11
36.6
Winter,
1961-62
18
12
40.9
14
28.9
Spring,
1962
10
9
28.2
11
R9.1
Summer,
1962
11
3
13.9
10
43.6
infestations
could
provide
a
parasite
reservoir
to
supple-
ment
populations
in
neighboring
citrus
groves,
particu-
larly
during
periods
of
light
scale
infestation
on
citrus.
The
rapid
establishment,
increase,
and
natural
spread
of
holoxanthus
in
Florida
is
most
encouraging
and
indi-
cates
that
this
parasite
may
become
an
important
factor
in
the
biological
control
of
Florida
red
scale.
REFERENCES
CITED
DeBach,
Paul.
1960.
The
importance
of
taxonomy
to
biologi-
cal
control
as
illustrated
by
the
cryptic
history
of
Aphytis
holoxanthus
n.
sp.
(Hymenoptera.:
Aphelini-
due),
a
parasite
of
Chrysomphalus
aonidum
(L.),
and
Aphytis
coheni
11.
sp.,
a
parasite
of
Aonidiella
aurantii
(Maskell).
Ann.
Ent.
Soc.
Amer.
53:
701
-
5.
Muma,
Martin
H.
1959.
Natural
control
of
Florida
red
scale
on
citrus
in
Florida
by
predators
and
parasites.
Jour.
Econ.
Ent.
52:577
-
86.
Muma,
Martin
H.,
and
D.
W.
Clancy.
1961a.
Parasitism
of
purple
scale
in
Florida
citrus
groves.
Florida
Ent.
44:
159-65.
Muma,
Martin
H.,
and
D.
W.
Clancy.
1961b.
Parasitism
of
purple
scale
and
Florida
red
scale
in
Florida
citrus
groves.
Proc.
Florida
State
Hort.
Soc.
74:29-32.
Simanton,
W.
A.
1960.
The
reduced
status
of
purple
scale
as
a
citrus
pest.
Proc.
Florida
State
Hort.
Soc.
73:
64-9.
The
Mating
Behavior
of
the
Boll
Weevil,
Anthonomus
grandie
M.
S.
MAYER?
and
J.
R.
BRAZZEI)
ABSTRACT
The
mating
habits
of
the
boll
weevil
were
studied
to
determine
the
percentages
of
those
mating
in
various
age
groups
and
time
interval
between
repeat
mating.
The
numbers
of
males
mating
increased
as
their
ages
increased.
The
length
of
the
interval
of
confinement
and
the
age
of
the
female
had
less
effect
on
the
per-
cent
increase
of
mating
than
the
age
of
the
male.
Observations
indicated
that
the
female
would
attempt
to
re-
pulse
the
male
if
she
had
been
mated
within
24
hours
prior
to
the
mating
attempt.
Males
were
found
to
mate
more
frequently
than
females.
Analyses
were
made
of
certain
biological
phenomena
of
nonmated,
once-mated,
and
multiple-mated
females.
Nonmated
females
laid
a
high
percentage
of
eggs
on
the
outside
of
the
cotton
square,
while
mated
females
deposited
the
majority
of
eggs
inside
the
square.
The
females
which
were
mated
only
once,
laid
eggs
normally
for
approximately
19
to
21
days
and
then
re-
verted
to
an
unmated
behavior
pattern.
The
successful
use
of
the
"sterile
male"
technique
in
eradication
of
the
screw-worm
(Cochliontyia
hominivorax
(Coquerel))
in
the
Southeastern
United
States
has
stimu-
1
Contribution
No,
4230,
Texas
Agricultural
Experiment
Station,
in
co-
operation
with
the
Entomology
Research
Division,
AIRS,
USDA.
Accepted
for
publication
November
27,
Mi.
2
Research
assistant,
Entomology
Department.
3
Professor,
Entomology
Department.