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This is a progress report only. Information herein reported should not be published without consent of the project leader.

BIOLOGICAL CONTROL OF THE NAVEL ORANGEWORM

AGRICULTURAL EXPERIMENT STATION PROJECT 1983 - H

ALMOND CONTROL BOARD RESEARCH PROJECT 74-F

1975 ANNUAL REPORT

prepared by

L. E. Caltagirone

University of California Department of Entomological Sciences

Division of Biological Control, Albany

Correct Project Number 75-F2

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TITLE: Biological Control of the Navel Orangeworm.

PERSONNEL:

a) Permanent (U. California funds)

L. E. Caltagirone, Project Leader (~ time)

D. W. Meals, Staff Research Associate (full time)

b) Temporary (Almond Industry funds)

Mabel Fong, Staff Research Associate (~ time)

Alice Wu, Staff Research Associate (~ time)

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I. OBJECTIVES AND GOALS: The principal objective is to control the

navel orangeworm by means of natural enemies - parasites and predators­

so as to reduce as much as possible its economic importance as a pest.

To achieve this we have endeavored

to determine what natural enemies of the navel orangeworm

are already present and what influence these enemies have

upon the pest population,

- to explore for natural enemies, including pathogens in

the home environment of the pest, and to introduce these

into California, and

- to evaluate the effectiveness in controlling the abundance

of the navel orangeworm by such natural enemies as are

successfully established.

The immediate goals were:

- to evaluate the establishment and impact of the parasite

Pentalitomasti~ plethoricus in the areas where it had

been colonized,

to explore for additional natural enemies, and

- to gather data on nav.el orangeworm populations as they

occur in almond orchards.

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II. ABSTRACT: The parasite Pentalitomastix plethoricus, known to the

almond growers as the "almond wasp", is established in almond orchards

in Chico and vicinity (Butte Co.), Le Grand and Snelling (Merced Co.),

and Famoso (Kern Co.). During 1975 releases of this parasite were

limited to Capay (Yolo Co.) and Lost Hill (Kern Co.). It has been

recovered from both localities: from Capay in only trace numbers, while

samples from Lost Hill reveal a 14% parasitization of the NOW larvae

at harvest time. We do not know yet whether it is definitively

established in these areas.

Samples from Chico indicate that this parasite successfully

overwintered in 1974-75, and that it has increased its level of

destruction of navel orangeworm. Harvest time samples indicate that

in some orchards 44% of the navel orangeworm population has been

destroyed.

Intensive sampling in Snelling indicates that in this area

the "almond wasp" is also doing extremely well. During 1974 the wasp

was colonized in some 800 acres of the 1469 acres planted to almonds

in the L D Properties Ranch. Samples of the overwintering navel

orangeworm population (worms in the old nuts) show that the parasite

has destroyed from 37% to 80% of the pest in the sections where it was

colonized. Such high levels of mortality will result in fewer navel

orangeworm moths in these orchards this coming season.

Two other parasites, one from Israel (Phanerotoma flavites­

tacea), and the other from Mexico (Parasierola sp.) were colonized in

Yolo Co., Merced Co., and Kern Co. They have been recovered from the

release areas, but it is too early to say whether they are established

or not.

Some areas in Texas and New Mexico were explored for natural

enemies of the navel orangeworm. No NOW infestations were found. One

parasite that may attack NOW was found and imported to California.

Its usefulness against the navel orangeworm is yet to be determined.

ased on our 1975 work, the almond wasp seems to have

become an important mortality factor against the navel orangeworm.

We expect to determine its capabilities to bring about economic control

of the pest during the 1976 season.

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III. EXPERIMENTAL PROCEDURE:

1.- Laboratory culture of parasites.

a) Pentalitomastix plethoricus.- This parasite was discovered

in Mexico and imported to California. The females search. for and sting

navel orangeworm eggs; an egg is then laid in the NOW egg, which is not

killed. The NOW larva hatches and develops apparently normally, but it

carries the parasite inside. When the NOW larva has completed its

development it spins a silken cocoon. At this time the parasit$inside

the NOW larva develop very quickly killing the host, of which only the

outer skin is left. The parasites transform into adult wasps inside

the dead NOW larva. This parasite is a polyembryonic one, that is,

from a single egg many adults develop; in this case an average of

500 adult Pentalitomastix develop inside each parasitized NOW larva.

Based on these biological characteristics, ~. plethoricus

is mass cultured as follows:

-Navel orangeworm eggs are exposed to female Pentalitomastix

for some 24 hours,

-These parasitized eggs are placed in 1-gallon containers ~

full of a rearing medium consisting of a mixture of wheat

bran, brewers yeast, honey, glycerine, and water.

-After the NOW larvae have spun their cocoons the parasitized

larvae are collected and prepared for colonization in the

field and/or for stock to continue lab culture.

b) Phanerotoma flavitestacea, and~. inopinata.- Phanerotoma

flavitestacea was imported from Israel where it parasitizes the carob

pod moth, Ectomyelois ceratoniae. f. inopinata is native to California.

Both species have similar biologies, and the culturing method is the

same for both. Females search for and sting ~avel orangeworm eggs

where and eggs is laid. The NOW larva hatches, apparently. unharmed by

the parasite it carries inside. After the NOW larva completes its

development and spins its cocoon, the parasite develops at a fast rate

consuming the host, leaving only the head capsule and part of the

integument (skin). Soon after, the parasite larva spins its cocoon

inside the NOW cocoon. Eventually the parasite energes as an adult

cutting its way out of the two cocoons.

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To culture these species, the Mediterranean flour moth,

Anagasta kuehniella, is used as a factitious host. This moth is

easier to culture than the navel orangeworm. The procedure is as

follows:

- Mediterranean flour moth eggs are collected from oviposition

units and sprinkled on wet paper. When the paper dries,

the eggs remain stuck on it. These eggs are exposed to

parasites for oviposition for about 24 hours.

- The parasitized eggs are placed in 1 gallon jars ~ full

of a culturing medium composed of chicken feed (starter

and laying), rolled barley, raisins, and glycerine.

- When adult parasites emerge, they are collected and used

for field colonization, and/or to keep the culture in

the lab.

c) Paraolinx typica.- This parasite is native to California.

The females search for and lay eggs on NOW larvae in the nuts; medium

size to full grown larvae are preferred. Prior to laying the eggs the

female parasite permanently paralyzes the host larva. Upon hatching,

the parasite larvae feed on the paralyzed NOW larva, leaving only the

head capsule and the integument. After reaching full size the parasite

larvae turn into pupae, and soon after into adults.

To culture this parasite, nearly full grown navel orangeworm

or Mediterranean flour moth larvae are exposed to the parasites. The

parasitized larvae are then transferred to glass jars where the new

generation adults emerge. These are collected for field colonization

and/or for continuation of the colony in the lab.

d) Parasierola sp.- This species was imported from Mexico.

Its biology is very similar to that of Paraolinx typica. Females search

for, paralyze, and lay eggs on nearly full grown NOW larvae in the nuts.

Larvae of the parasite feed on the paralyzed NOW larva.

To culture this parasite, large Mediterranean flour moth or

NOW larvae are exposed to the parasite females. In this case one larva

is exposed to one female, since when they are kept in large groups in

a single container, the parasites interfere with each other. This results

in high mortality of the parasites, and low parasitization.

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2.- Colonization of parasites in the field.

Pentalitomastix plethoricus was colonized placing

mummified parasitized navel orangeworm larvae in screened 2 oz.

condiment plastic cups hung in the trees. Generally some 20 to 25

parasitized larvae were placed in each cup •. As some 500 adult

parasi tes develop in each parasitized larva, ani allowing for a

natural mortality (failure to emerge from the parasitized larva) of

28%, a total of 7200 to 9000 adults are released in each colonization

point. In the 1974 season the parasite was colonized in the L D

Properties Ranch in Snelling, Merced Co. at the rate of one colonization

point every tenth tree every fifth row.

The other parasites were taken or sent to the orchards as

adult, and were released for them to disperse themselves.

3.- Analysis of navel orangeworm populations.

The navel orangeworm spends all its developmental stages

- egg, larva, and pupa - on or in the almond nuts. This makes it

possible to treat each nut as a sampling unit. To assess population

density, age distribution, and percentag~ of kernel damage, as well as

the impact of navel orangeworm parasites, samples of some 200 nuts

are periodically taken. Sometimes samples are smaller because of

unavailability of nuts. Harve~samples consist of larger number of

nuts (1000 or more). In the laboratory each nut is examined for

eggs viable

larvae

pupae

emerged

parasitized by Trichogramma

viable

parasitized by Pentalitomastix

Parasierola

Paraolinx

dead due to other causes

viable

emerged

The number in each category is recorded. The viable eggs,

larvae, and pupae are reared in medium and the final status of the

individuals (parasitized or unparasitized) is finally recorded. A

tally of the number of nuts examined (size of the sample) and of the

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number of damaged kernels is kept. Thus the level of navel orangeworm

infestation, and the structure of the popu~ation of navel orangeworm

and its parasites in each nut is known.

IV. RESULTS:

1.- Colonization of natural enemies.- Colonization of

natural enemies, mostly parasites, was a reduced activity during the

1975 season. The different species, and the localities in which they

were colonized are indicated in Table I below.

Table I. Colonization of natural enemies of the navel

orangeworm in 1975.

Natural enemy Locality No.

colonized Total

Pentalitomastix plethoricus

Phanerotoma flavitestacea

Phanerotoma inopinata

Paraolinx typica

Parasierola sp.

Haplothrips sp.*

Swanson Orchard, Capay 2,J39,264 Yolo Co.

Blackwell Land Co., Lost Hill, Kern Co. 8,398,512

Delantico Orchard, Oakley, Contra Costa 220,320 10,758,096

L D Properties, Snelling, Merced Co.

Swanson Orchard

Blackwell Orchard ,

L D Properties

Swanson Orchard

Swanson Orchard

Blackwell Orchard

Swanson Orchard

Blackwell Orchard

Swanson Orchard

1.,156

6,498

5',175

793

85

13,800

2,000

2,890

3,950

470

12,829

15,800

6,840

470

Total natural enemies colonized 10,794,913

* predator

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2.- Establishment, and impact of Pentalitomastix plethoricus

on navel orangeworm populations.- Sampling of navel orangeworm populations

has confirmed that this parasite is now established in Chico and vicinity

(Butte Co.), Oakley (Contra Costa Co.), Le Grand and Snelling (Merced

Co.), and Famoso (Kern C9.). It was also recovered from Capay (YoloCo.)

and Lost Hill (Kern Co.), but since parasites were colonized in these

localities in 1975, it is premature to say whether the parasite is

established there.

Harvest samples from the Blackwell Land Co. Orchard, Lost Hill,

reveal that 14% of the navel orangeworm population in ~he colonization

area has been destroyed by K. plathoricus. This level, reached during

the first year of colonization is higher then the first year in Chico

(7%), and Snelling (11%).

Old and new nuts were collected in th~ Chico area where the

parasite has not been colonized since June 1974, and examined to

determine parasitization. Table II contains the information gathered.

Table II. Parasitization of navel orangeworm by Pentalitomastix

plethoricus in the areas indicated. All samples

collected in 1975.

Orchard

Nottelmann, Hegen Rd. Chico

Nottelm~, Fimple Rd. Chico

Carter, Chico

Seever, Chico

Hanson, Chico

Decker, Durham-Dayton Rdo

* old nuts

** new nuts

Sampling date

23 July

10 Sept.

23 July

23 July

23 July

23 July

23 July

No. nuts % examined parasitization

150* 46.2

1 168** , 44.7 169* 32.2

167* 52.3 226* 37.3 222* 36.9 220* 23.6

Analysis of the data collected in the Nottelmann Orchard on

Hegen Rd., Chico, indicates that the impact of the parasite on the navel

orangeworm population has been steadily increasing from 7% in 1971 to

44.7% in 1975 (Fig. 1).

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Intensive sampling of the L D Properties Ranch, Snelling,

where Pentalitomastix plethoricus was not released in 1975, was

conducted in most of the sections of the 1469 acres planted to almonds.

During the previous season (1974) the parasite was distributed in

about 800 acres (Fig. 2). Analysis of the samples revealed that the

parasite has become established, and that it is inflicting high

percentages of parasitization in some sections. Results obtained up

to this writing are presented in Table III.

Date sampled

10 April

27 Feb.

15 Dec.

15 Dec.

10 April

8 May

25 June

25 Aug.

3 Nov.

27 Feb.

15 Dec.

Table III. Analysis of almo~d nuts collected in the L D

Properties Ranch, Snelling. All samples

collected in 1975.

No. nuts % nuts with via­examined ble eggs, larvae

and/or pupae

440*

160*

180*

292*

260*

93*

198**

200**

237*

223**

,

Section F-29

22.5

Section F-30

14.4

pending

''-' Section F-31

pending

"'- Section F-32

3.4

2.3

"-I Section F-34

5.4

14.6

pending

Section F-36

6.8

pending

No. viable eggs, larvae , and/or pupae per 100

nuts

36.1

20.6

pending

pending

4.1

2.3

23.7

22.2

pending

10.6

pending

% parasitism by Pentalitomastix

o

o recovered

recovered

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9.5

3.7

pending

o pending

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Table III. (continued) (

Date No. nuts % nuts with via- No. viable eggs, % parasitism by sampled examined ble eggs, larvae larvae, and/or Pentalitomastix

and/or pupae pupae per 100 nuts

Section F-38

8 May 293* 12.6 19.5 11.5

25 June 353* 15.6 49.0 28.5

17 Sept. 372** pending pending 38.5

4 Dec 198** pending pending pending

Section F-39

8 May 218* 16.1 32.1 11.1

Section F-41

10 April 250* 31.6 66.0 18.1

8 May 202* 141.9 28.2 22.7

10 July 229* 21.8 60.7 34.3

7 Aug. 168* 42.3 167.9 55.3

( 25 Aug. 188* 31.9 83.5 58.7

25 Aug. 179** 27.4 55.9 58.4

3 Nov 202** pending pending 66.8 (prelim.)

Section F-43

10 April 263* 22.1 37.3 6.3

25 June 257* 18.3 80.9 18.9

7 Aug. 170* 30.6 114.1 29.8

25 Aug. 225* 19.1 41.8 60.0

25 Aug. 159** 6.3 11.3 33.3

17 Sept. 1048** pending pending 37.3

Section F-44

15 Dec. 209** pending pending pending

15 Dec. 270** pending pending 80.4 (prelim.)

'Section F-45

16 Jan. 526* 33.7 52.5 18.0

21 Feb. 361* 33.8 55.1 17.0

10 April 300* 25.0 41.3 18.1

8 May 330* 36.7 72.7 13.4

25 J1.me 200* 35.0 13.0 35.8

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Table III. (continued)

Date sampled

10 July

7- Aug.

17 Sept.

3 Nov.

4 Dec.

* old nuts

No. nuts examined

202*

200*

1128**

200**

204**

** new nuts

% nuts with via­ble eggs, larvae and/or pupae

No. viable eggs, larvae, and/or pupae per 100

nuts

Section F-45 (continued)

21.3 75.2

27.5 102.0

23.9 41.3

pending 183.5

pending 165.7

% parasitism by Pentalitomastix

48.3

43.6

80.2

79.7 (prelim.)

72.5 (prelim.)

Figure 3 depicts the progression of parasitization by

Pentalitomastix in Section F-45 and F-41 , L D Properties Ranch, Snelling.

3.- Establishment of other natural enemies.- Phanerotoma

flavitestacea has been recovered from L D Properties, Snelling, and from

Swanson Orchard, Capay. Parasierola sp. has been recovered from Blackwell

Ranch, Lost Hill, and from Swanson Orchard. No statement can be made

regarding the establishment of these species in these areas.

The predaceous thrips Haplothrips sp., which was released

only in the Swanson Orchard, has not been recovered; presumably it did

not establish itself.

4.- Exploration for natural enemies.- From 22 September

to 3 October 1975 exploration in search of navel orangeworm and its

natural enemies was conducted in Texas and New Mexico. Plants known

to be hosts for the navel orange worm - including almond, apple, apricot,

peach, pecan;' plum, walnut, fig, acacia, yucca, and soap tree - were

examined in EI Paso and surroundings, and Davis Mountains in Texas,

and in the area from Las Cruces to Santa Rita, and Carlsbad in New

Mexico. No navel orangeworm was found, but three parasites, considered

to be worthy of investigation were collected and brought to California.

They were processed according to quarantine regulations. Two of the

parasites, both in the family Eulophidae, did not reproduce in quarantine,

while the third, a species of Bethylidae in the genus Goniozus parasitized

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successfully larvae of the Mediterranean flour moth. This parasite will

be tested against navel orangeworm when enough number of adults are

secured.

v. DISCUSSION:

We have determined that there are some 11 species of

natural enemies of the navel orangeworm in California. Of these, the

parasite Pentalitomastix plethoricus is the only exotic, the others

are parasites of other insects that are native, or have been in California

for a long time. These natural enemies do not seem to have the potential

to reduce navel orangeworm populations to non economic levels on their

own. The possibility to improve their effectiveness by manipulation

(inundative and/or inoculative releases, additional food sources, etc.)

have not been investigated.

Pentalitomastix plethoricus, on the other hand, is having

a great impact on the navel orangeworm , especially in Chico and Snelling,

the two areas where this parasite has been more intensively colonized.

The levels of parasitization in these areas indicate that the number of

parasites overwintering in the orchards is extremely high; they should

have an even greater impact on the pest this coming spring. For example,

in Nottelmann Orchard, Regan Rd.,Chico, the level of parasitization is

44 percent. This means that next spring of every 100 navel orangeworm

larvae, 56 will develop into adult moths, and 44 will produce parasites;

but since each parasitized larva produces an average of 500 parasites,

there will be 22,000 parasites, or a projected 393 adult parasites for

each navel orangeworm adult. The situation in certain areas in the

Snelling L D Properties Ranch is even better. In Section F-45, for

example, the level of parasitization is 80 percent, or a projected

2,000 adult parasites for every navel orangeworm adult come next spring.

Pentalitomastix plethoricus disperses very slowly - ~ to

~ mile per year - while the navel orangeworm disperses much more

rapidly. This is why it has not yet been possible to determine the

potential of this parasite to reduce the damage caused by the moth.

To know this potential the parasite should be distributed in a large

area, so that the whole resident navel orangeworm population is subjected

to the effect of the parasite. This condition seems possible to occur

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next season in the L D Properties Ranch in Snelling, which is a

somewhat isolated orchard. Once the potential of this parasite is

determined in one area, it will be possible to choose the strategy,

or strategies to disperse it or to manipulate it more efficiently in

other areas.

The remarkable increase in parasitization in Chico and

Snelling, where no Pentalitomastix were released in 1975, suggests that

this species has become well adapted in these areas. We do not discount

the possibility that an adaptation of this parasite to California

conditions has occurred, or is occurring. The logical step to take is

to move this parasite from Chico, Snelling, and Le Grand to other

areas, especially to those in which the parasite was released in past

years, but where we have failed to recover it.

Intensive monitoring of the navel orangeworm and Pentalitomasti~

populations in Chico, Le Grand, Snelling, and Lost Hill - to the extent

permitted by the resources available -, and transfer of parasites from

these to other locations in California should be the main activity of

this project for the coming season.

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