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1BIOLOGICAL CONTROLOF INSECT PESTS

B~ C. P. CLAUS~N
Vni~ersit.yof California,Riverside,California
Control of agricultural insect pests by the biological methodhas made
remarkable strides during the past 25 years, and an adequate treatment of
the subject necessitates coverageof at least that period rather than the five
or ten years to which manyother reviews are limited. Manyprojects are of
long duration and there is frequently considerable delay in the publication
of final results. The last general review of the subject was that by Sweetman
(96). Becauseof the space limitations, this review will deal only with the
utilization of insect parasites and predators in control of crop pests, and the
rapidly expanding field of microbial control, wherein disease-producing or-
ganismsare utilized for the samepurpose, will not be considered here. Like-
wise, the subject of the effect of chemicalcontrol practices uponpopulations
of parasites and predators, which has becomeof great importance since the
advent of DDTand other high toxic’chemlcals, and the means whereby
these harmful effects can be alleviated, will be excludedfrom consideration.
The very large number of biologlcal-control projects that have been
undertaken during the period under review makesit impossible even to list
them, and those selected comprise pest species with which the outcomehas
been highly successful or which demonstrate techniques or phenomenathat
are of special interest to workersin this field. It is noteworthythat, as in the
past, the greatest attention has been given to the scale insects, mealybugs
and white flies, and the successes in control have been more numerouswith
the homopterouspests than with species of other orders.
Unfortunately, detailed reports are not available regarding manyim-
portant projects, other than a brief statement of the final general outcome.
General reviews of the status of biological control in the various countries
are available in only a few instances, these being by Clausen (17) for the
continental United States, Pemberton(77, 78) for Hawaii, O’Connor(75)
for Fiji, Jenkins (59) for WesternAustralia, Miller el al. (69) for NewZealand
and Kamal (60) for Egypt.
RESULTS OF BIOLOGICAL CONTROL

Coconutmoth, Levuanairidescens Bethune-Baker.--Oneof the outstand-

ing examplesof biological control of a lepidopterous pest is that on the coco-
nut moth in Fiji, accomplishedthrough the introduction of a tachinid fly,
PtychomyiaremoraAldrich, and reported uponin detail by Tothill et el. (104).
Field control of the pest was accomplishedin manyareas within six months
after release of the parasite, and economiccontrol was general throughout
~ Thesurvey of the literature pertaining to this reviewwascompletedin June,
1957.
291
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292 CLAUSEN
the Islands within two years. Field releases of insectary-reared material
totalled 32,570, mainlyparasitized host larvae. Several factors were highly
favorable for this successful outcome.The life-cycle of the parasite is very
short in relation to that of the host, and the adults have exceptional powers
of dispersion, having negotiated in one instance a flight of 12 miles over
water. Further, the mild ,climate of Fiji throughout the year, and the over-
lapping generations of the host, provide optimumconditions for uninter-
rupted increase.
A noteworthyfeature of this project is that t’t~,chomiyia, native to Ma-
laya, is a normal parasite of another genus and species, Artona catoxantha
Hampson. In the history ,~f biological control, instances of successful utiliza-
tion of parasites from another host genus are exceedingly rare.
Oriental fruit moth, Grapholitha molesta (Busck).--This pest is nowat-
taining worldwidedistribution and large-scale efforts in biological control
have been undertaken in the United States and other countries. A large
numberof parasite species were introduced into the United States from Japan
and China (50) but only one, Agathis diversus (Muesebeck), becameestab-
lished, and that at only a very few points. Greater success was attained
through use of a native parasite, Macroc~ntrusanc:ylivorus P, ohwer, which
adapteditself to this host. Widedistribution of this parasite resulted in high
parazlt|zatlon in most areas, accompaniedby a marked reduction in fruit
infestation (119). Similar results are reported from Canada(108). The
troduction of Macrocentrusinto other countries, such as Australia, France,
Italy, Argentina, and Brazil have not been effective, possibly because of lack
of a suitable alternate host.
Brunson & Allen (12) found that mass releases of Macrocentrus at an
average rate of 330 per acre in NewJersey, in seasons whenthe native popu-
lation was inadequate, resulted in a reduction of approximatelyone-half in
fruit infestation.
Macrocentruswas employedwidely in one phase of the unsuccessful at-
tempt to eradicate the oriental fruit moth in California during the early
1940’s whenmorethan z.t8 million were released in infested orchards during
a three-year period (35). This was on an inundative basis, the releases often
far exceeding in number:~the pest populations in the orchards. Field recov-
eries were madethe season of release, but the parasite failed to becomeestab-
lished in that state, thoughthe pest itself has persisted, but at a generally
low level, in several areas.
Codling moth, Carpoc.apsa pomonella (Linnaeus).--The attempts to con-
trol this pest biologically have centered mainly on the use of the egg para-
sites, Trichogramma spp. Somereductions in fruit infestation are reported
for the United States (1) and Spain (106), while in Russia substantlal reduc-
tions were obtained in orchards having heavy infestations (85), but other
tests havebeen inconclut~ive. All experimentshave involvedrelease of several
thousandparasites per tree. In general, the results obtained against fruit in.
sects have not been sufficient in the extent of control or consistency to war.
rant recommendationfor the use of this parasite by growers. Larval para-
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BIOLOGICAL CONTROLOF INSECT PESTS 293

sites, mainly Ascogaster quadridentata Wesmaeland Mastrus carpocapsae
(Cushman)have been tested in several countries, but without success.
Coconut spike moth, Tirathaba triehogramma Meyrick.--An extensive
programfor the biological control of this pest in Fiji was carried on for a
number of years. The details of the importation and colonization program
are given by Paine (76), whoreports four parasite species from Java as es-
tablished, the most important being Apanteles tirathabae Walkerand Erycia
basifulva Bezzi. The injury by the pest, premature nutfall, was checked, al-
though control was not complete (64).
Oriental moth, Cnidocampaflaveseens (Walker).--The introduction and
establishment of the taehinid fly, Chaetexorista javana Brauer &Bergstrom,
into Massachusettsresulted in full control of the oriental mothexcept dur-
ing seasons following exceptionally cold winters. This exampleillustrates
strikingly the differential effect that maybe exerted uponhost and parasite
by low temperatures. It was found by Dowden(29) that winter temperatures
below0° F. are lethal to the second-instar parasite larvae in the hibernating
host prepupae, yet the unparasitized hosts are not affected. A minimum
temperatureof - 19° F. in 1933resulted in a field parasitization of less than
10 per cent the following season, but the normal high parasitization was re-
gained in following years.
Imported cabbageworm,Pierls rapae (Linnaeus).--A substantial reduction
in infestations of the eabbageworm, thoughnot consistent field control, is re-
ported from NewZealand by Muggeridge (70). This was accomplished
the pupal parasite, Pteromaluspuparum(Linnaeus), and field parasitization
often approaches100 per cent.
Sugarcane borer, Diatraea saceharalis (Fabridus).--Extensive efforts
have been madein manyof the countries of the Western Hemisphereto con-
trol the sugarcane borer by the biological method. The earlier attempts were
in the use of the egg parasite, Trichogram~na minutumRiley, and reductions
of crop loss of 50 per cent are reported by Tucker (105)in Barbadosand sub-
stantial reductions by Smyth(93) in Peru and Wolcott &Martorell (116)
Puerto Rico. A detailed series of experiments in Louisiana by Jaynes &
Bynum(58) involving releases of up to 45,000 Tricho~ramraaadults per acre
resulted in no benefit whatever. Theseconflicting results maywell be due to
differences in climate and cultural practices, cane being an annual crop in
Louisiana.
The introduction and establishment of the Cubanfly, Lixophagadiatraeae
(Townsend),in southern Florida resulted in partial control, the parasitiza-
tion often amountingto 65 per cent or more, aided in someareas by Agathis
aigmaterus (Cresson) (83). Climatic conditions, especially unusually
winters, are adverse to the parasites, so that there is a wide fluctuation in
parasitization fromseason to season, and recolonization is at times necessary.
The introduction of Lixophagainto St. Kitts in the WestIndies resulted in a
substantial reduction in borer injury (8).
The Amazonfly, Metagonistylum minense Townsend has been very
widely colonized and has becomeestablished on several islands of the West
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294 CLAUSEN
Indies, with a considerable degree of conti’ol reported on the island of St.
Lucia(7).
Larchsa~vfly, Pristiphora eriehsonii (Hartig).--The biological control of
the larch sawfly in Canadathrough the introduction of Mesoleiustenthredinis
Morleyfrom England in 1910-11was highly successful for a period of years
thereafter, but a decline in effectiveness of the parasite was noted in Mani-
toba beginning about 1940. A detailed study by Muldrew(71) of the factors
responsible for this situation revealed that, in Manitobaand Saskatchewan,
the pest has developed a pronouncedimmunityto successful parasitization
by Mesoleius. Dissections of parasitized larvae showed that more than 90
per cent were able to destroy the embryobefore hatching, this being ac-
complishedby phagocytic action resulting in encapsulation of the developing
egg. Noevidence of immunitywas found in material from British Columbia,
but the parasite has been established in that province only since 1934-36.
Recent observations by Drooz (31) in NewYork reveal a fairly high para-
sitization, with no evidence of physiological resistance, so that the phenom-
enon is at present limited to the areas of earliest establishment.
This situation has serious implications in biological control of crop pests,
though fortunately it appears to be an isolated case, and a comparableloss
in field effectiveness of a parasite species has not heretofore been recorded.
One wondersif this developmentin the Pristiphora-Mesoleius relationship is
a selection process wherebythe susceptible elements in the population have
been progressively eliminated and is therefore analagous to the development
of resistance to insecticides by manypest insects.
Europeanspruce sawfly, Diprion hercyniae (Hartig).--The biological con-
trol of this pest in eastern Canadahas been one of the largest scale projects
to date. During the 1930’s and continuing into the following years, a large
series of parasites was irnported from Europe and manywere successfully
established (4, 80). Speci~dattention was given to the pupal parasite, Dahl-
bomlnusfuscipennls (Zetterstedt), of which hundreds of millions were re-
leased each year. Manyof these parasites were later released in infested
states, especially Maine, in the United States and Dahlbominusbecamees-
tablished (30). In the early 1940’s an epidemic outbreak of a virus disease
the larvae developedand in a few years greatly reduced the infestations in
all areas. The final outcomeof the parasite release programwas for that rea-
son obscured. Unfortunately, an over-all account of this project has not yet
been published, though manyarticles have dealt with individual elements in
the parasite complex.
Coconutleaf-mining be.ale, Promecothecareichei Baly.--The work on the
coconut leaf-mlning beetle in Fiji is an outstanding but rare exampleof
successful biological control of an endemicinsect pest. Originally an economic
balance had been maintained between the pest and its natural endmies, but
this balance was upset big the accidental introduction of a predacious mite,
Pediculoides ventricosus Newport, into the complex. This mite caused the
periodic elimination of all developmentalstages of the host and thus evened
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BIOLOGICALCONTROLOF INSECT PESTS 295

the successive generations of the beetle in contrast to the overlappingof the
generations so essential to the continuedeffectiveness of the native parasites.
Taylor’s (98) detailed account of this problemand its solution presents sev-
eral points of special interest.
Before undertaking foreign exploration for effective natural enemies, the
situation was reviewed and an analysis madeof the attributes required of
the parasites to accomplish control under the changedconditions mentioned
above. A search was then madein Java for parasites fulfilling those require-
ments. PleuraropisparvulusFerriere, an internal parasite of all of the larval
stages and of the pupa as well, the normal hosts of which are other species
of Promocaheca in Java, appeared to meet all requirements. Its introduction
into Fiji and the early release of a total of 25,900adults resulted in complete
economiccontrol in less than one year. Other successful efforts for the con-
trol of hispid leaf-miners have been on Brontispa frogatti selebensls Gestro by
Tarastichodesbrontispae Ferriere, a larval-pupal parasite, in Celebes (3) and
on Bronlispa marianaSpaeth in the Palau Islands by the same parasite (26,
62).
Eucalyptus snout weevil, Gonipterus scutellatus Gyllenhal.--Thls snout
weevil is native to Australia and has spread to manycountries in which
eucalyptus is grownfor timber purposes. It becameexceedingly destructive
in South Africa, and biological control efforts, beginning in 1926, resulted
in the importation from Australia in that year and the establishment of an
egg parasite, Anaphoideanitens Girault. The recent detailed account by
Tooke(103) of progress on this project, covering the period from 1926
1950, with its extendedconsideration of all factors bearing uponreproduction
and increase of host and parasite, is one of the outstanding contributions to
biological control in recent years. Too often, successes are reported only
briefly, without details as to production techniques, field observations, etc.
The parasite brought about rapid and full economic control in all of
southwestern and southern Cape Province and generally in most other areas
below 4000 ft. elevation. Mild winters with mean minimumtemperatures
not below48° F., with winter or all-year rainfall were found to be most favor-
able for parasite effectiveness. In highland areas, such as occur in the Trans-
vaal and Natal, the cold and dry winters retarded control, as both conditions
prevent host oviposition for several months in the spring and thus shorten
the period of activityof the parasite, and the populations fluctuate accord-
ingly. Overall, the parasite has shownits adaptability to an unusually wide
geographic and climatic range.
The host has 2 to 23 generations each year and each female deposits 180
to 270 eggs, whereasthe parasite has 5 to 6 generations and deposits 25 to
50 eggs, thus permitting very rapid build-up. Dispersion of the parasite is
rapid, instances having been noted of spread of more than 20 miles in three
monthsand 100 miles in a single season. Effective control was accomplished
on 63 of 65 species of eucalyptus grownin South Africa.
This is one of the exceedingly few instances of a pest insect being con-
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296 CLAUSEN
trolled by an egg parasite alone. It has generally been assumedthat egg para-
sites represent a mortality factor of relatively minorimportance, as they are
seldomable to destroy a sufficiently high portion of the host eggs to have a
dominantinfluence on the host population.
Since its introduction into South Africa in 1926, A. nilens has been in-
troduced into and established in Argentina, Kenya, Madagascar,Mauritius,
NewZealand, and RhodesJla, in several of which, notably NewZealand (69),
Madagascar(49), and Mauritius (114), it has been equally as effective as
South Africa.
Fruit flies (Tephritidae).--Investigations on the biological control of
fruit flies of the family Tephritidae have beenconductedin several countries,
with the major efforts centered on the Mediterranean fruit fly, Ceratitis
capitata (Wiedemann);the oriental fruit fly, Dacus dorsalis Hendel; and
the melonfly, Dacuscucurbitae Coquillett, in the HawaiianIslands (18). The
early work on the Mediterranean fruit fly during 1912-16 resulted in the
establishment of five parasite species, of which Opius tryoni (Cameron)from
Australia was the most effective, and brought about a substantial reduction
in infestations in certain fruits, especially coffee.
Opiusfletcl~eri Silvestri, the parasite of the melonfly importedfromIndia,
has not had an appreciable influence on the host infestations, and recent
studies by Newellet al. (72) and Nishida (73) reveal that its activities,
represented by the percentage of parasitization are muchreduced during the
summermonths. Fruit infestation is nowhigher and parasitization lower than
reported by Willard (113) for the period shortly after introduction of the
parasite.
The appearance of the oriental fruit fly in Hawaiiin 1946led to a very
large parasite importation program, in the course of which 4,246,000 puparia
of that and about 60 other species of the family were imported for parasite
rearing (18). Elevenspecies and varieties of parasites are knownto be estab-
lished and field parasitization nowaverages 70 to 75 per cent. Field infesta-
tions have been reduced substantially, thoughchemical control methodsstill
need to be employedin commercialorchards and gardens. The changing rela-
tive status of the three major parasite species, as reported by van den Bosch
&Haramoto(107,), is of special interest. Opius longicaudatus malalensls
Fullaway, the first established, very quickly attained a high rate of para-
sitization, but was superseded the following year by O. vandenboschiFull-
away. The latter in turn was replaced a year later by the egg-larval parasite,
O. oophilus Silvestri. This last species has been, virtually alone, responsible
for the continuedhigh parasitization since 1950. Its effectiveness is enhanced
by a fungous disease of the host eggs that is transmitted by the parasite fe-
males when ovipositlng.
Mealybugs (Pseudococcidae).~The mealybugs as a group appear to be
especially amenableto biological control. The early introduction of Cryptol-
aemusraontrouzieri Mulsantand Leptomastideaabnormi~(Girault) into Cali-
fornia led to partial control of the citrus mealybug,Planococcuscirri (Risso),
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BIOLOGICALCONTROLOF INSECT PESTS 297

and later, in 1928, the complete control of the citrophilus mealybug,Pseudo-
coccus gahani Green, was achieved by Coccophagus gurneyl Compereand
Tetracnemuspretiosus Timberlake(20). So effective were these latter para-
sites that it has becomedifficult to find even a single specimenof the host
in the citrus orchards. The long-tailed mealybug, Pseudococcus adonidum
(Linnaeus), on avocado was likewise controlled in that state by Anarhopus
~ydneyensis Timberlake and Tetracnemus peregrinu~ Timberlake, imported
from Australia (41).
The Comstock mealybug, Pseudococcus comstocki (Kuwana), a pest
several deciduous fruits, has spread from Japan to manyparts of the world.
Its principal parasites, Allotropa burr¢lli Muesebeck,Pseudaphycusmalinus
Gahan, and Clausenia purpur¢aIshii, the first two imported into the United
States in 1939-41, have been effective in bringing about economiccontrol in
practically all states, typical being the outcomein Ohioas reported by Cut-
right (21). Published accounts for other states are not yet available. Accord-
ing to Rivnay(82), a substantial reduction of what is questionably consid-
ered to be P. eornstocki on citrus in Israel has resulted from the importation
and establishment of C. purpurea.
Anextended programfor the biological control of the coffee mealybug,
Planococcuskenyae Le Pelley, was undertaken in Kenyafrom 1925 onwards,
though large-scale efforts were conductedby Le Pelley (63) during 1936and
following years. Becauseof uncertainty as to the identity of the pest, the
search for its natural enemiesextendedto manytropical and subtropical re-
gions of the world, but effective species adapted to it were found only in
nearby Uganda and Tanganyika. Anagyrus kivuensis Compereproved to be
the most effective, aided in some localities by Anagyrus sp. and Pauridea
peregrina Timberlake. Full economiccontrol was not attained in all infested
areas, thoughsubstantial reductions in infestations, crop losses, and cost of
treatment were brought about.
A large-scale effort has been under way since 1948 on the Gold Coast of
Africa for the biological control of Pseudococcusnjalensis Laing, and a large
series of parasites has been imported from manyparts of the world (110).
This project is of particular interest because the objective is control of the
swollen shoot disease of cacao, a virus disease of whichthe mealybugis the
vector. The normal population of the mealybug is low, as compared with
infestations of the more.commonspecies on citrus and deciduous fruit trees
in other countries, and the population needs to be reduced to such an ex-
tremely low level to provide control of the disease that the problembecomes
exceedinglydifficult. The chanceof success is consequentlygreatly reduced.
Citrus blackfly, Aleurocanthus woglumiAshby, and other Aleyrodidae.--
The citrus blaekfly, native to tropical Asia, has becomea serious pest of
citrus and other trees in tropical and subtropical Americasince its discovery
in Jamaicain 1913. Oneparasite, Eretmocerusserius Silvestri, and a predator,
Catana clausenl Chapin, both from the Malayanregion, were imported and
established in Cuba (19). Full economic control was accomplished very
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298 CLAUSEN
quickly, not only in Cubabut in other West Indian Islands, and the Panam
Canal Zone and Costa Rilca as well. This was through Eramocerusalone,
though Catana demonstrated a capacity to reduce heavy infestations very
quickly. It is unable to persist in light infestations, however,and, therefore,
has little value in holding infestations at a low level. Its highly specialized
habits, limiting feeding to the eggs and first-instar larvae, preclude its main-
taining full control without the aid of other natural enemies.
After the finding of the citrus blackfly in Mexico,a cooperative project
between the agricultural organizations of that country and the United
States was set up to undertake biological control. Eretmocerus serlus was
imported and established but proved to be ineffective because of adverse
climatic conditions. Additional species of parasites were then imported from
India and Pakistan during 1948-50 and became established, these being
Amitus hesperidurn Silvestri, Prospaltella clypealir Silvestri, Prospaltella
opulenta Silvestri, and Prospaltella smStki Silvestri. Thedistribution program
has been the largest of any similar project, hundredsof millions of these par-
asites being colonized annually. According to H. D. Smith (89), economic
control has been achieved in practically all parts of the country, with the
exception of small areas on the West Coast. Amitus has been most generally
effective, while the several species of Prospaltella have been able to control
the pest under special and limited conditions.
A related blackfiy species, Aleurocanthus st~nlferus Quaintance, was
brought under control in. Japan by Prospaltella smithi (61), and in Guam
Amitus hesperidum and P. smithi (79).
The methods originally developed by Speyer (95) for the production
the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and its
parasith, Encarsia formosa Gahan, have permitted effective and economical
biological control of the pest in greenhouses. The whitefly is producedon a
mixedstock of tomato and tobacco. The latter plant, being unattractive to
the parasite, maintains a high whitefly population from which the tomato
plants are continuously’ infested, and the parasitized whiteflies from that
plant are utilized for distribution. Effective control of the pest has been re-
ported in England, Australia (I02), Canada(66), and Belgium.
Coconutscales, Aspidiotus destructor Signora and others.--The most im-
portant of the scale insects attacking coconut in manytropical areas is A.
destructor, and a detailed accountof the highly successful efforts to control it
biologically in Fiji has been presented by Taylor (97). A considerable num-
ber of parasite and pr~lator species were imported from Java and Trinidad
and several of the predator species becameestablished. A single coccineIlid
species, Cryptognatht~ nodiceps Marshall, was highly effective and very
quickly brought the pest under full economiccontrol in all islands of the
group.
C. nodiceps is considered to have several qualities that contribute to an
exceptional degree to field effectiveness, amongthem being its specialized
feeding habit in both the larval and adult stages, long adult life, a high re-
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BIOLOGICALCONTROLOF INSECT PESTS 299

productive capacity, and remarkable powers of dispersion. Other factors
contributed to the high degree of control attained, one of the most important
being the gregarious or colonial habit of the host, which provides adequate
food for the immaturestages of the beetle, with a minimum of searching re-
quired, and second, and perhaps most important, the mild climate of Fiji
which permits reproduction throughout the year.
The success with Cryptognathain Fiji led Taylor to state that "Parasites
have invariably failed as complete and permanent controls for scales" and
"as a general rule it is desirable to seek predators rather than parasites for
the control of a scale which, like A. deslrudor, does its damageonly by severe
outbreaks." It is unquestionablytrue that the highly specialized predators,
such as Cryptognatha,Catana, and Rodolia, are very valuable, but the number
of such species is small and the great majority of scale insects do not have
predator enemiesof similar capacity. The successes with parasites of scale
insects, mealybugsand whiteflies have nowgreatly exceededin numberthose
by predators alone.
Other scale insects are destructive to coconut in various parts of the
world, and in the Seychelle Islands the two most important species are
Pinnaspis buxi (Bouch6)and Ischnaspis Iongiroslris (Signoret). A series
predators was imported during 1936-38, of which the most effective proved to
be Chilocorusnigritus (Fabrieius) fromIndia. A survey of the field situation
by Vesey-Fitzgerald (109) in 1952revealed that C. nlgritus had reduced veiy
substantially the infestations in the Islands, resulting ia a markedincrease
in nut production.
California red scale, Aonidiella aurantii (Maskell).--Workon the biologi-
cal control of the California red scale, a destructive pest of citrus, has been
under wayin California for sixty years, yet it was only after the introduction
of Aphygs lingnanensis Competefrom South China in 1949 that appreciable
results in control have been attained. This outcomehas been limited, how-
ever, to the coastal area. Periodic releases, totalling 100,000 or moreper
acre each year, have yielded economiccontrol in several intermediate cli-
matic areas where the natural population was ineffective (25). The red scale
race of Prospaltella perniciosi Tower, obtained from Formosa,showsconsid-
erable promise.
Theclosely related yellowscale, A. dlrlna (Coquillett), is adequatelycon-
trolled in southern California by the Japanese race of Comperiellabifasciata
Howard,obtained from Aonidiell~ on Podoct;rtms, but is ineffective against
the pest in the San Joaquin Valley (44).
Juniper scales, Carulaspis visd (Sd;rank) and Lepidosaphes newsteadi
~ule.--An extensive programfor the biological control of these two destruc-
tive pests of Bermudacedar, Juniperus bermudiana,was undertaken in 1947
by the Commonwealth Institute of Biological Control. Thompson(101) re-
ports that of 30 to 35 species of parasites and predators introduced, only two
becamewell established, these being Lindorus lop,nine (Blaisdell) and
Microweiseasuturalis Schwarz. In spite of high parasitization byAspidioti-
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300 CLAUSEN
phagusand heavy feeding by the coccinellids, the programwas unsuccessful
because of the extremelylethal effects of even small populations of scale upon
the trees.
Olive scale, Parlatoria oleae (Colv~e).mThebiological control program
on the olive scale in California serves to illustrate several problemsthat may
confront workers in this field. Stocks of Aphytis maculieornis (Masi) im-
ported in 1951 from the area extending from India through the Middle East
to the Mediterranean proved to be indistinguishable morphologically, yet
studies by Hafez & Dout:t (51) revealed the existence amongthem of three
races or sibling species that have been designated as the Indian, Persian, and
Spanish forms, and which show distinct biological differences. Underfield
conditions in California th.e Persian form has provento be mosteffective. The
results obtained in this study emphasizeonce again the need for obtaining
stocks of each parasite species from all parts of its geographicrange, rather
than from only a single source.
Doutt (27) reports that Apkytis increased rapidly in the experimental
orchards in whichit was ~:eleased and often attains a parasitization of 90 per
cent or more of the spring brood of scales. Attack upon the summergenera-
tion is always low, very seldom exceeding 20 per cent. The general scale
population on the trees in the years following parasite release was substan-
tially less than 10 per cent of that occurring previously, so that, on the basis
of ordinary criteria, the trees were commerciallyclean. It developed later,
however,that the few remaining scales of the second generation were largely
concentrated on the fruit. Thus the fruit injury, which is the main cause of
loss from this pest, is reduced very muchless than the reduction in numbers
of the pest itself.
Fig scale, Lepidosaphesficus (Signoret).--The apparently successful con-
trol of this pest of figs and other plants is another instance of the occurrence
of host-determined races of a parasite species. The one involved, Aphytis
mytilaspidis (LeBaron), occurs as a parasite of Lepidosaphesthroughout the
United States, but in California it parasitizes only a very small proportion of
the fig scales. The importation and colonization of stocks of this parasite
from fig scale in Italy resulted in high field parasitization and apparent
economiccontrol at the release sites (28, 48, 56).
Pustule scale, Asterolecaniumpustulans Cockerell.~This pest of certain
shade and forest trees i.n Puerto Rico was so completely controlled by the
introduced Chilocorus cacti Linnaeus that specimens of the ~eale could not
be foundover a period of 12 years after general establishmentof the predator,
though it has since been taken in small numbers(115).
Black scale, Saissetia oleae (Bernard).~Prolonged efforts to find effective
natural enemiesfor the control of the black scale in California finally resulted
in partial success when Aphycus helvolus Competewas obtained from South
Africa in 1937 (90). This parasite has proven to be most effective in the
coastal areas where the "uneven hatch" condition of the host prevails and
wherewinter temperatures are milder than in the interior valleys. Protracted
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BIOLOGICALCONTROLOF INSECT PESTS 301

cool periods in these valleys during the winter are often followed by heavy
scale infestations. Whilefull or partlal economiccontrol of the scale on citrus
is effected by Aphycusunder favorable conditions, yet it is noteworthy that
in no instance has the parasite been effective against this pest on olives in
the San Joaquin and SacramentoValleys. A byproduct of the extensive dis-
tribution of Aphycusagainst the black scale was its complete suppression of
a related species, Salssetia nigra (Nietner), a pest of shade and ornamental
trees in southern California.
The introduction of the several black scale parasites into other countries
has given variable results. In southern Peru, for example,whereS. oleae was
a serious pest on olive, the infestations were brought under control by
A phycus launsburyi Howard,Scutellista cyanea Motschulskyand Lecan~obius
utilis Compere(6). This outcomemust be attributed mainly to Apkycus as,
on the basis of observations in California, the egg predators, even whenvery
abundant, contribute very little to reduction of the infestations.
2~ed wax scale, Ceroplastes rubens Maskell.--The red wax scale became
one of the most destructive pests of citrus and other fruit trees and shrubs in
Japan following its appearance in that country about sixty years ago. Sev-
eral parasites were knownto attack it, though in very small numbers, but
this situation changed rapidly after 1946, when Yasumatsu (117) found
that a highly effective parasite had appeared in FukuokaPrefecture and
was spreading rapidly. It was first determinedas Anlcetus ceroplastls Ishil
but later described as a newspecies, A. beneficus Ishii &Yasumatsu.Follow-
ing this discovery the parasite was reared in large numbers and widely
distributed, and economiccontrol has already been attained in manyareas
of Kyushu and Honshu.
There are several possible explanations of the sudden appearance of A.
beneficus in Japan, and Yasumatsu(118) expresses the belief that it may
have arisen by mutation from the native A. ceroplastis. This explanation,
of course, cannot arbitrarily be excluded, though such a development has
not heretofore been observed within the parasite complexof any other pest
insect. Asecondpossible explanationof the situation is that A. beneficusis a
recent accidental introduction from abroad, presumably from China, but
this too is at present questionable inasmuchas the species has not thus far
been represented in any of the numerouscollections of Anicetus from the
Asiatic mainland.
Cyclamenmite, Steneotarsonemuspallidus (Banks).MThebiological con-
trol of phytophagousmites presents exceptional difficulties and, on the basis
of our present knowledge, the prospects cannot be considered encouraging.
Someprogress has been made on the cyclamen mite problem on strawberries
in California, where Huffaker & Kennett (57) have demonstrated a method
whereby control maybe accomplished through manipulation of native pre-
daceous mites, Typhlodromus cucumeris Oudemans and Typhlodromus
reticulatus Oudemans.Old fields normally have high populations of the
predator a~l distribution of clippings from normal winter pruning into in-
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302 CLAUSEN
rested
fieldsgavegoodcontrol.
Itissuggested
thatequilibrium
ofpestand
predator
maybe attained
early
in eachplanting
ifdeliberately
stocked
with
bothduring
thefirstgrowing
season.
RESEARCHP, ELATINGTO BIOLOGICAL CONTROL
Massproduction of parasites and predators.--The work and cost involved
in the insectary rearing of parasites and predators employedin manybio-
logical-control programshas been very greatly reduced, in manyinstances,
through the development of mass production methods. Whenpracticable, it
permits production to meet any colonization program in a minimumof time
and also, at an economically practicable figure, in numberssufficient for
periodic or inundative release programsagainst certain types of pests. In
somecases, wherethehoststageto beparasitized is inactive, suchasthe
eggsofthegypsy mothandthose of therangecaterpillar, orthecocoons of
theEuropean spruce sawfly, thehostmaterial canbe.collected inthefield
invirtually unlimited quantities, andtherearing of parasites presentsno
particular problem. Itismoredifficult, however, whensapfeeders, suchas
scale insects andmca[ybugs, fruit feeders,suchasthefruit flies andcodling
moth,andstemborers areinvolved. Obviously, it wouldbe economically
impracticable to produce therequired numberon thenormalfoodplantof
suchpestinsects. Thegeneral subject of culture ofentomophagous insects
hasrecently beenreviewed by Flanders (4S).He concludes (47)thatin
production programs theincrease to be expected underany economical
method is aboutequalto theaverage number of eggsdeposited perdayby
theparasite female.
In themassculture of entomophagous insects themainproblem usually
is concerned notwiththeparasites or predators themselves butwiththe
hostinsects. It maybe solved by (a)theproductidn of thehoston plant
parts, suchas melons, tubers, etc.,thatarenotnormally infested inthe
field; (b)theutilization ofa factitious host(86)amenable torearing on
plantparts, thatisacceptable to theparasite or predator; and(~)thede-
velopment ofartificial foodmediaforhostorparasite.
Potato sprouts havet~roven to besuitable fortheproduction of various
mealybugs (91)andtheblackscale(38)whilethetubersthemselves
excellent fortheproduction of California redscale(46), latania scale,and
manyotherdiaspine scaleinsects (43).Thefruits of various Cucurbltae,
especially squash andcitron, serve fortheproduction ofCalifornia redscale
(39), SanJosescale (40), oleander scale, andmanyotherS. Ripeoranges
foundtobesatisfactory fortheproduction of six-spotted mites
Examples offactitious hostsutilized inparasite rearingprograms arethe
Angoumois grainmothand otherstoredgrainpestsproduced in cornor
wheat for the production of the egg parasites, Tri~hograraraaspp. (36, 94),
the Mediterranean flout" moth for rearing of Chelonus and Bracon species
(10, 74), the potato tuberwormin potatoes for the production of Macro-
~entrus ancylivorus (35), a parasite of the oriental fruit moth, a~d the eggs
and larvae of the tuberworm for production of the predator, Chrysopa
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BIOLOGICALCONTROLOF 1NSECT PESTS 303

plorabunda Fitch (32). Manyof the parasites of dipterous puparia may
readily reared in puparia of Drosophila,house flies, blowflies, etc.
The costs of mass production of hosts and parasites maybe greatly re-
duced through measures developed to obtain maximumreproductivity of
the species involved. Synthetic foods for the adults mayserve this purpose.
It was found by Hagen(52) that egg deposition of Chrysolmplorabunda was
greatly increased by adding an enzymatic hydrolysate of brewer’s yeast to
the honey solution fed to the adults. With host insects, Hagen& Finney
(53) report that fecundity of the oriental fruit fly wasvery greatly increased
through the use of the same food supplement.
The formulation of synthetic food mediafor the parasites themselves, as
a substitute for the normal insect host, has intrigued manyworkers in the
past, though little research was done on the problem. The complex nutri-
tional requirementsof both endo- and eeto-parasites, as well as the changing
physical conditions required as development progresses from egg to pupa,
seemedto present insurmountabledifficulties. The parasitic species of the
dipterous family Sarcophagldae, present possibly the simplest problem, and
it was one of these, Pseudosarcophaga a~nis (FaIl6n), parasitic in the spruce
budworm,Choristoneurafumiferana (Clemens), that was the subject of study
by House &Tract (55). It was found that a food mediumconsisting of pork
liver and fish was fully acceptable to the larvae and that a muchhigher pro-
portion reached maturity on this mediumthan on the normal insect host.
This permitted year-round production of the parasite in any desired quan-
tity, a great advantage whendealing with a univoltine host. House’s later
workon this sameparasite has dealt with a wide range of essential nutrients.
The developmentof synthetic food media for the host insects has shown
considerable promise. Ripley et al. (81) found that the false codling moth,
Argyroploce leucotreta Meyrick, would develop and reproduce readily on a
preparation of oatmeal porridge lightly infected with the mold Mucor
hiemalis Wehmer.In Hawaii, enormous numbers of the oriental and other
fruit flies were producedOn a mediumof blended fresh squash fortified with
additional essential nutritive factors (67). Later modificationof this method
provided for use of fresh carrot (34) and then of commerciallyavailable de-
hydrated carrot (13), which permits of year-round production independent
uncertain supplies of the fresh product.
Various meansmaybe employedto replace the laborious rearing of host
material and to insure an ample supply throughout the production program.
In the rearing of the aphid-feeding coccinellid, Hippodamiaconvergens
Gu6rin, Haug(54) found that this could be readily accomplishedthroughout
the year by the use of frozen aphids. The species used was the poplar petiole
gall aphid, Pemphiguspopuli-transversus Riley. The poplar galls containing
the aphids were stored at -21 to -250 C. and remained in good condition
for manymonths. For storage purposes this aphid was more satisfactory
than those occurring on open foliage because of the greater ease of handling
of the galls containing them and less rapid decomposition and desiccation
after removalfrom storage.
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304 CLAUSEN
Devices for the automatic collection of host or parasite serve to reduce
the cost of mass production programs. Examplesare the units developed by
Spencer et el. (94) for rearing and collecting adults of the Angoumois grain
moth and the trap described by Bedford (5) for collecting Chelonustexanus
Cresson in the rearing rooms. The latter methodutilizes two light sources,
the first being daylight fluorescent tubes behind a landing screen, from which
surface the parasites are then attracked t~ natural daylight into suitable con-
tainers.
Biological studles.--A knowledgeof the biology and habits of the ento-
mophagousspecies (15) being utilized in biological control is obviously
value, thoughnot alwaysessential, in biological control programs.Occasion-
ally, however, such knowledgeprovides the key to success of an entire pro-
gram. This was strikingly illustrated by the discovery by Flanders (37) Cf the
phenomenon of sex differentiation in the host relations of a series of Coc-
c@hagusspecies parasitic in scale insects, wherein the females develop as
primary parasites and the males as secondary parasites. This habit, since
found to occur in other genera of Aphelininae, makesnecessary special tech-
niques in field colonization to effect establishment. After this discovery, it
becameclear whya numberof earlier attempts to establish certain parasites
of scale insects, mealybugs,and white flies had been unsuccessful.
The existence of biological and host-determinedraces, as mentionedin the
discussion of the olive scale and others, has very muchcompllcated the de-
velopment to completion of manybiological control projects. To date, the
problems have involved mainly species of Eulophidae and Encyrtldae para-
sitic in scale insects, but the occurrenceof such races is knownin other groups
and is probably muchmorefrequent than is realized at present.
The possibility of developing newraces or strains of parasite species,
adaptable to specific climatic or other conditions, has intrigued biological
control workers for many’years, but only recently has this been attempted
on an adequate basis. I~. studies on the developmentof cold-hardiness in
Dahlbominusfuscipennis(Zetterstedt), Wilkes (Ill) found that the.average
temperature preferendum of both sexes is between 21.2 and 22.8 ° C., with
two minor peaks at 1.5 ° C.. and 9° C. In midsummer three nearly equal groups
preferred temperatures of 25, 15, and 9° C., respectively. Continuousselec-
tion gave a markedincre.ase in the percentage of individuals preferring the
lower temperatures. An adaptive process in nature has produced the same
results as those obtained by artificial selection in the laboratory. The breed-
ing of strains with specific preferenda mayhave considerable practical value
in the field colonization program. Very few entomophagousinsects are
adapted to the full climatic range of their hosts, manybeing limited to only
a small portion of that range.
Preliminary experiments by Box (9) using the cane borer parasites
Metagonistylum minense Townsendand Paratkeres~a claripalpis (van der
Wulp) appear promising. Races of Paratkeresla from Trinidad, Mexico,
Venezuela and Peru were crossed, and the resulting hybrid from Venezuela-
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BIOLOGICALCONTROLOF INSECT PESTS 30~

Trin|dad pa~ents appeared to be the most vigorous and possibly best suited
to Venezuelanconditions.
Evidencepresented by Allen (2) indicates that a parasite species maybe-
comeadapted to a host to which it initially was not attracted, Workingwith
Horogenesmolestae (Uchida), a parasite of the oriental fruit moth, he found
that it could be induced to parasitize potato-tuberwormlarvae only in the
presenceof larvae of its normalhost. After several years of insectary rearing,
however, it developed a high attraction for that host; the production in
pure cultures of tuberwormlarvae being 24 times that attained in the first
tests. The question then arises as to whetherthis host-adapted strain retains
its original attraction to its normalhost whenreleased in the field.
The sex ratio of laboratory stocks,--The problemof maintaining a favor-
able sex ratio in laboratory stocks is an important aspect in the economical
massproduction of manyparasite species, Onseveral projects the proportion
of females in these stocks has declined progressively to the point whereade-
quate numbersof females could not be produced, or the ratio of females be-
cameso low that even maintenancewas impossible. By a process of selective
breeding Wilkes (112) was able to demonstrate that this developmentcan
reversed. A selective breeding program with Dahlbominusfuscipennls re-
ducedthe incidence of sterile males from 35 percent to 2 per cent and at the
same time increased the mean numberof progeny per female from 38 to 68.
These findings contributed substantially to the more economicalproduction
of the manymillions of Dahlbominusutilized in the Europeanspruce sawfly
program.Simmonds (87) reports similar results in the rearing of the codling-
moth parasite, Mastrus (Aenoplex) carpocapsae (Cushman).
Martin & Finney (68) improvedthe sex ratio of Macrocentrusancylivorus
by decreasing the light intensity in the mating roomand by allowing a 24-hr,
emergenceperiod. They also found that the ratio of females increased with
the degree of superpara~sitization. FIanders (42), working with the same
parasite, found that multiple mating mayresult in prevention of fertiliza-
tion of the female and reduced oviposition through crowding of spermato-
phores in the vagina.
Thesize of the host often has a very definite influence on the sex ratio of
the parasite (14). This was strikingly demonstrated by Brunson(11) in
case of Tiphia popilliavora Rohwer, parasitic on the larvae of Popillia
japonica Newman.Those developing on second-instar grubs were predom-
inantly males, whereas on third-instar grubs the ratio was reversed. Mc-
Gugan(65) found that the males of Apechthis ontario (Cresson) emerged
mainly from male host pupae and females from female pupae, apparently
the result of selective oviposition. Obviously,this factor of host size needs to
be considered in developing techniques in some mass production programs.
Evaluationof parasite andpredatoreffectiveness.mAgreat deal of difficulty
has been experienced in evaluating the effectiveness of introduced or native
natural enemies. Someprogress has been madein this respect with those at-
tacking scale insects and mealybugs in California. Smith &DeBach(92)
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306 CLAUSEN
demonstrated that enclosure of infested branches in bags of fine-meshed
cloth, to exclude the natural enemies, permitted a comparison of host de-
velopment and increase with and without them. This study was later ex-
tended and modified by DeBach(22) in which trees were sprayed with DDT
and talc, those treated with DDTshowing a great increase of long-tailed
mealybug while the trees receiving talc or no treatment showed a very
markeddecline in pest populations, due mainlyto the activities of predators.
The cloth sleeve-test methodmentionedabove was later modified (24)
combinethe features of both methods, the sleeve enclosing the branches be-
ing impregnated with technical DDT,and held in such a way as not to be in
contact with the foliage. Checksleeves were untreated and open at both ends,
permitting normal activity of natural enemies.
The question arose later as to the possible stimulating effect of repeated
light applications of DDTon the pest insects themselves. It was shown(23)
that such application had no appreciable effect upon populations of Cali-
fornia red scale or yellow scale. The insecticidal check methodoffers a ready
meansof evaluating the effectiveness of natural enemiesof pest species such
as scale insects, mealybugs,and possibly whiteflies and mites.
The tlme.factor in biological controL--Thequestion of the length of time
required for introduced parasites and predators to demonstrate their capac-
ity for control of a pest in the field has long been of interest and concern to
entomologists engagedin biological control activities. Becauseof the small
numbersof the beneficlalt species released in relation to the large population
of the host, it had been asserted frequently that a long interval is required
before the full effectiveness of the introduced natural enemiesis attained.
This subject has been discussed by Clausen (16), whoreviewed, insofar
detailed published data are available, all instances of what is generally ac-
cepted as full commercialcontrol. These data indicated, without exception,
that fully effective parasites and predators demonstrate very quickly their
capacity for control of their hosts, and that this is achievedin the immediate
area of release within three years, a period often representing only three host
generations. This conclusiondoes not apply to partially effective parasites as
their activities are strongly influenced by changingenvironmentalinfluences.
A species destined to be fully effective is always easily and quickly estab-
lished and, conversely, the failure to becomeestablished easily and quickly is
a definite indication that it will not be fully effective later. Variousaspects of
this problem are presertted in criticisms of the above article by Thompson
(100) and Sellers (84)
THE PRESENT STATUS OF BIOLOGICAL CONTROL

Anyanalysis of the present status of biological control of insect pests and

a projection of developmentsinto the future are of muchinterest and reveal
a wide divergence of opinion, even amongexperts in the field. A provocative
discussion of the subject is that by Taylor (99) whotakes a definitely pessi-
mistic viewpointas to the possibility of worthwhileachievementsin this field
in the future, indicatinlg that the cream has already been skimmedawayand
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BIOLOGICALCONTROLOF INSECT PESTS 307

the point of diminishing returns has long since been reached. Simmonds (88)
presents a vigorous rebuttal to Taylor’s thesis and cites manyexamplesto
illustrate the points at issue. Space limitations prevent an adequate review
of these two articles, but a few points maybe mentioned.
Taylor states
¯ .. I knowit [biological controll to be the best of all methodsof controllingpests
whenit works,but that it seldomworksand that there is little future for it in con-
tinental areas.
The successes in North Americaalone during the past 25 years are sufficient
rebuttal to that statement. Systematic work in biological control of insect
pests has hardly started in the great majority of continental countries, and
there is every reason to expect results in those countries comparableto the
successes achieved in North America and elsewhere. Accordingly, we may
expect substantial progress in manyareas in future years. Further,
¯.. the present tendencyto organize the movingof parasites and predators about
the worldon an ever-increasingscale, despite deereaslngresults, is unsoundandis,
therefore, to be regretted.
A weighingof results of such recent workcertainly refutes the assertion of
decreasing returns.
The somewhat outmodedidea that insular conditions are in some way
conducive to success in biological control is dealt with at somelength by
Taylor. That the most frequent successes in biological control have been
attained on tropical islands is obvious from the record. These islands (Ha-
waii, Fiji, etc.) are characterized by a year-round equable climate, lacking
cold winters and hot dry summers,and conditions are ideal for uninterrupted
development of the natural enemies. Anydeparture from that ideal situa-
tion obviously reduces the chances of success. Hibernation, summeralia-
pause, lack of alternate hosts, etc., enter into the picture, any one of which
factors maycause a reduction in effectiveness or even prevent establishment
of a natural enemy that under more favorable conditions would be fully
capable of controlling its host. The greater degree of success in tropical
island areas maybe attributed, not to insularity as such, but to (a) optimum
climatic conditions for development and increase of the natural enemies,
and (b) the pest species occurring there are practically all of foreign origin
and lack effective native control agents.
The need for intensive study of the ecological relationships of host and
parasite is emphasized by both Taylor and Simmondsthough qualified by a
realization of the difficulties involved in supporting such researches on an
adequate basis. At the present time, it is difficult to visualize the mannerin
which these detailed ecological studies can contribute substantially to the
practices of applied biological control, insofar as the parasite introduction
programsare concerned. For example, it is extremely doubtful that detailed
studies of Erelmocerusserius Silvestri of Malaya,which so successfully con-
trolled the citrus blackfly in the West Indies, would have revealed, in
either or both countries, its completeineffectiveness after establishment in
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3O8 CLAUSEN
Mexico. Taylor’s pronouncement to the contrary notwithstanding, biologleal
control today is very largely on an empirical basis and will remain so for
many years to come.
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1. Alden, C. H., and Webb,J’. E., Jr., Georgia State Board Entomol, Bull. No.
79, 23 pp. (1937)
2. Allen, H. W., J. Econ. Entomol., 47~ 278-81 (1954)
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4. Baird, A. B., Ann. Rept. Entomol.Soc. Ontario, 70, 51-56 (1940)
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BIOLOGICAL CONTROL OF INSECT PESTS 309

39. Flanders, S. E., J. Econ. Entomol., 36, 233-35 (1943)
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