iological control involves discover- Citroph ilus mealy bug B ing, importing, and using the most effective natural enemies of pest insects Second only to cottony cushion as a or weeds that can be found. More than 10 success story for biological control is the million natural enemies of many kinds citrophilus mealybug campaign in Cali- are released each year by the University fornia. of California (UC) through its Biological In the 1920s citrophilus mealybug Control divisions at Albany and Riverside. was a spreading scourge in citrus orchards. UC scientists estimate that the It was highly destructive, it spread rapid- importation and release of biological con- ly, and it affected other fruit trees and trol agents in California alone has saved ornamentals. The mealybug’s origin was producers and consumers of food and fiber a mystery, but UC scientists deduced it about $300 million in the last half century. must have come from a climate similar Worldwide, the importation of natural to that of southern California and from a enemies has brought about some degree place linked by steamer to England, of control of 186 species of pest insects; South Africa, and California, the three there have been 384 successful projects places where the mealybug was known. in biological control of pest insects to date. This pointed to Sydney, Australia. In this review, “biological control” Harold Compere, a UC biological (BC) refers to only one of the many non- control scientist, was dispatched to Aus- chemical insect control methods on which tralia in 1927. Within a year he found an UC scientists are working. BC is the im- infested mulberry tree on which virtually portation, colonization, and spreading of all of the mealybugs had been parasitized. natural enemies (usually from the ”old He collected two parasites, Gocrophagus country” where the pests originated) to gurneyi and Tetracnemus pretiosus, and reduce a pest’s population density to a accompanied them to California on the lower average than would otherwise steamship Tahiti. Both parasites were occur. colonized and released in 1928. In 1929 citrophilus mealybugs were already being decimated wherever the First success parasites had been liberated; by 1930 the parasites’ eggs laid inside mealybug lar- The first effective and sustained vae had resulted in complete economic success of biological control occurred in control. Since that time, no infestations 1888 against the cottony cushion scale, of any importance have occurred. Orange Zceryapurchasi. The scale attached itself County citrus growers alone saved $0.5 to leaves and twigs of citrus trees, then million to $1 million a year. The cost? sucked out the sap. Discovered in Cali- About $1,700, not including Compere’s fornia in 1872, it soon threatened to salary of $150 a month. destroy the citrus industry. Albert Koebele, a USDA ento- Conquering a weed mologist, was sent to Australia in 1888 Vcdalia, the iZustralian ladyhird beetle /Rodolia to seek a parasite that apparently was A classic example of biological con- cardinalis) feeding on cottony cushion scale trol was a joint UC-USDA campaign against lIwrl/a purrhasi). keeping the scale under control there. Koebele shipped 514 vedalia beetles (the Klamath weed (Hypericum perforaturn), Australian ladybird, Rodolia cardinalis) an accidental import from Europe. By to California, where they quickly became 1944 it occupied over 2,000,000 acres of established. rangeland in 30 California counties, By 1890 the vedalia had attacked crowding out range grasses. Livestock and almost obliterated all infestations in men suffered financial losses, because California. Cost of the vedalia program, cattle and sheep feeding on the toxic all told, was less than $5,000. Benefits? weed lost weight and because land values - Millions of dollars annually in California. decreased, making it hard to get loans Similar successes were scored with the for improvements. Chemical controls, ap- same beetle in more than 50 countries. plied against a mere trace of the total Unfortunately, DDT and other infested acreage by state and local govern- chemicals, used after World War 11, ments, cost as much as $300,000 a year. destroyed the vedalia in many areas. As early as 1922 Professor Harry Cottony cushion scale then re-emerged Scott Smith, head of biological control as a serious pest after 50 years of ab- work in California, proposed the impor- sence. The vedalia was recolonized after tation of insects that fed on the weed in the insecticide residues on tree foliage Europe. In 1944 Smith finally was author- Vedalia larva feeding on cottony cushion scale. had dissipated, and soon reasserted its ized to import four kinds of beetles and 10 times lifesize control over cottony cushion scale. a gall-forming fly from Australia and

8 CALIFORNIAAGRICULTURE OCTOBER 1977 Europe. After careful testing to ensure means has been difficult and costly. Its w a I n u t aphid. the beetles wouldn’t attack desirable thorns and seeds are picked up and spread Discovered near Fresno in 1934, plants, the four beetles - Chrysolina by tires and bare feet. the olive scale, Purlntoria oleue (Colvee), hyperici C. quadrigemina, C. varicLns, In 1961, UC and USDA bio-control soon threatened many household and and Agrilus hyperici-and the gallfly scientists imported two weed-attacking parkway plants as well as olive and de- were released. All except C. variuns be- weevils from Italy: Microlarinus lureynii ciduous fruit trees. By 1960, more than came established; C. quadrigemina was and M. lypriformis. The former infests 200 types of ornamental plants, 28,000 the most successful species. puncture vine fruits and destroys the acres of olive orchards, and Lhousands of From a single colony of 5,000 C. seeds; the latter attacks the stem and deciduous fruit trees in 26 counties in the quadrigemina beetles released in 1945- crown. The two weevils were fairly suc- Central Valley and parts of southern 46, more than three million beetles were cessful in attacking the ground-hugging California were infested. Olive scale not collected for redistribution in California weed, but they soon ran into trouble only attacks leaves, twigs, and limbs, hut in 1950. The beetles also were sent to from native American insects. Two tiny also infests olive fruits, causing heavy Washington, Oregon, Idaho, Utah, Nevada, wasps attacked and destroyed about one- losses. The olive industry spent millions and Montana, where they became es- quarter of the young weevils in test of dollars fighting the pest. tablished. plots; two other native insects destroyed In the late 1940s. UC scientists By 1955 Klamath weed virtually the weevil eggs. As a result, weevil des- introduced natural enemies of olive scale. disappeared as a pest. Chemical control truction of puncture vine was cut in half. Only an Aphytis parasite from Egypt sur- costs dropped from $300,000 to less than Seeds of puncture vine can live in the soil, vived, but in small numbers. Other enemies $300 a year. Land values went up again. where weevils can’t get at them for 20 of olive scale were sought in Spain, Pakis- As range grasses reappeared, animals years or more. Even if two-thirds of the tan, India, and the Near East. Of four stopped losing weight. UC scientists seeds are destroyed before they mature, Aphytis strains imported, the most suc- estimate that savings to the livestock in- the remaining third can present a control cessful was a “Persian” strain of Aphytis dustry plus savings in control costs have problem. rnaculicornis from Iran and Iraq. Over been $3,500,000 per year, totaling about Despite these problems, the reser- the next eight years, more than 27 mil- $80,500,000 through 1976. voir of puncture vines seeds has diminished lion parasites of that strain were colonized In California, only Siskiyou County, over the last decade. In the presence of at hundreds of olive orchard sites in 24 with its very cold winters, still has a the imported weevils, now spread through- counties. Thousands were also released Klamath weed problem. Improved con- out California, puncture vine plants pro- on deciduous fruit trees, ornament a I trol has been obtained recently by the in- duce only about one-sixth as many spiny trees, and shrubs. troduction of a more cold-resistant C. hy- burs as they otherwise would.. Olive scale densities declined perici beetle and the root borer, Agrilus In another attack on weeds, on the dram B t i ca I I y , b ti t. scientists sought a hyperici, and by an apparent adaptive Channel Islands off Santa Barbara, UC higher degree of control than could he improvement of C. quadrigemina. scientists released a mealybug that achieved with the Persian Aphytis alone. sucked the juices out of prickly pear Although the Persian parasite often at- Puncture vine effort cactus, largely ridding the islands of this tacked and killed more than 90 percent of the olive scales in a given area in spring, Attempts to control puncture vine rangeland pest. (Tribulus terrestris) have been less suc- it failed to follow up in summer hcciiuse cessful than the Klamath weed project. Two recent successes of an intolerance to hot, dry weather and The control of puncture vine (long because of the absence of host (scale) a major pest around houses, roadways, The two most successful applica- stages during the late spring. ginning mills, vacant lots, and sometimes tions of biological control in recent years Two new species of aphelinid para^ on croplands) by chemical or cultural have been against olive scale and the sites were introduced from West F’aki-

Adult seed weevil (Microlarinus lareyniil on a seed pod of the Stem of puncture vine plant showing damage caused h) the stem wwvil. .Mrrrk puncture vine, nibulus ierrestris. 10 times lifesize larinus Iupriformis.

CALIFORNIA AGRICULTURE OCTOBER 1977 9 stan in 1957. CoccophagozdPs utilis Doutt and soon spread through all the walnut- tially eliminated as a pest of commercial thrived; the other species gradually dis growing areas of California. Frequently walnut groves. Streetside and garden appeared. it covered the trees, exuding honeydew trees also have benefited. A UC report By 1964, UC scientists found that on which a black, sooty-mold fungus grew. warns however: establishment of both A. maculicornis Years of insecticide war against the aphid “It is now most important in Califor- and C. utilis gave extremely effective produced the usual upsets, resurgences, nia walnut production that care be taken biological control of olive scale. 6. utilis resistance, and drift of toxic materials to avoid or prevent any factors or prac- took over from A. maculicornis in late outside treated areas. Biological methods tices which might disrupt the activity of spring and attacked whatever scales the seemed the only way to achieve real T. pallidus during summertime, since in- latter had missed. control. terference with the parasite may lead to Only 11 percent of California’s In the 1950s a UC researcher comb- explosive outbreaks of the aphid. The 28,000 acres of olive trees were treated ing southern France for an effective disruption is likely to result from insec- between 1971 and 1974. Currently, bio- parasite found a wasp with “high host ticidal treatments directed toward such logical control of olive scale is so thorough specificity”- that is, it went after the pests as codling moth or walnut huskfly. that it is almost impossible to find enough walnut aphid and no other insect. He im- The Argentine ant may also be disrup- of the pests to satisfy requests of foreign ported the French wasp (Trioxyspallidus ti ve .” entomologists asking for stocks of the Haliday), which spread rapidly through The report concludes: “Although scale’s parasites. The ravages of the coastal areas of southern California, lay- its activities may occasionally be disrupted scale on many species of shade and fruit ing its eggs inside the walnut aphid’s lar- by certain largely avoidable factors, T. trees and ornamentals also have been vae. Hatching wasp larvae then devoured pallidus has singlehandedly effected vir- eliminated. the aphid larvae. tually complete biological control of the The cost savings‘! Over a 12-year Although it wiped out a high per- walnut aphid in California.” period, UC scientists estimate, the olive centage of aphids in southern California, industry saved $7,260,000. The home- the French wasp couldn’t stand the heat Red scale: a long war owner, nurseryman, park keeper, and and dryness of central and northern roadway superintendent probably have California. A strain of T. pallidus from The campaign against red scale, saved even more. hot, dry Iran, was imported in 1968. Small Aonidiella aurantii (Maskell), has been releases of the new wasp developed into the longest in the history of biological The walnut aphid abundant populations that spread rapidly control. Since its arrival from the Orient and drastically reduced walnut aphids in the 1870s, red scale has been the chief The walnut aphid, Chromaphis jug- throughout California. pest of citrus and has caused losses of lundicola, invaded California about 1900 The walnut aphid has been essen- millions of dollars annually from damage

Olive scale parasite, Coccophagoides utilis, inspecting an olive scale’s C utilis perched on its host, top view. suitability to receive her egg.

Adult Tri~xuspullidus, a walnut aphid parasite, top view. A female T. pallidus thrusts her ovipositor into a walnut aphid, im- planting an egg which will develop into another tiny wasp, killing the host aphid.

10 CALIFORNIA AGRICULTURE OCTOBER 1977 to trees, loss in fruit quality, and cost of red scale. Although it is still a major and spread throughout southern Califor- insecticidal treatment. citrus pest and still requires chemcial nia, the wasps laid eggs inside the im- For 60 years, the biological control control treatments in most areas, its bio- mature nymphs of the woolly whitefly. effort against red scale was considered a logical control can be considered sub- The eggs hatched and grew into adults, failure. The parasite Aphytis chrysom- stantial. Many thousands of acres now go eating the whitefly in the process. phali Mercet did a fair job of controlling untreated each year, with enormous sav- Whitefly populations in release red scale in California’s mild coastal areas ings to the citrus industry. areas dropped by 90 to 99 percent. UC if not interfered with by chemical treat- scientists are able to stop new infesta- ments or by honeydew-seeking ants. But, Woolly whitefly tions by releases of parasites. since there usually were ants or chemi- Robert M. Boardman is Communications cals-or both-in citrus orchards, A. The woolly whitefly, a recent in- Specialist, University of California, River- chrysomphali was not highly regarded as vader from Mexico, has been so well con- side. Sources of information and aufhori- a natural enemy of red scale. In addition, trolled by UC-imported parasites that it ties consulted: Paul DeBach, Professor of there was a misconception about other has not had a chance to become a pest in Biological Control and Entomologist, Aphytis species that were available. All California’s commercial citrus. This is University of California, Riverside; known forms were assumed to be the in- probably the first instance of prophylac- Richard L. Doutt, Professor of Entomology, effective chrysomphali type. Inadequate tic (advance)biological control of pests. Emeritus, Biological Control, Parlier; taxonomy (identification) of the genus When uncontrolled, the whitefly Richard L. Goeden, Associate Professor Aphytis caused a delay of some 50 years sucks sap from leaves and secretes a of Biological Control, UC, Riverside; in the introduction of the most valuable waxy filament (with a woolly appearance) Kenneth S. Hagen, Professor of En- parasites into California and elsewhere. that covers the bodies of the nymphs tmnology, UC, Berkeley; Carl B. Huflaker. Between 1941 and 1957, UC scien- clustering thickly on the underside of Projessor of Entomology, UC, Berkeley; tists imported four species of parasites leaves. The nymphal and pupal stages of Charles E. Kennett, Specialist, Biological from India, West Pakistan, south China, the insect exude a sticky honeydew in Control, UC, Berkeley; Robert van den and Formosa. In order of effectiveness which sooty mold fungus grows. The fila- Bosch, Professor nf Entomology, UC, these were: two Aphytis species, A. ments and the fungus restrict the tree’s Berkeley; and the late James K. Hollo- melinus DeBach and A. lingnanensis photosynthetic action. The tree goes into way, US.Department of Agriculture en- Compere, and two red scale host races of a decline and fruit quality is lowered. tomologist. DeBach’s Biological Control Comperiellu bifasciata Howard and Pros- Three wasps, Amitus spiniferus, by Natural Enemies (Cambridge Univer- paltella perniciosi Tower. Eretmocerus paulistus, and Cales noacki sity Press, 19741 also provided valuable Parasitization by these four natural were imported from Mexico, Chile, and historical and statistical information. enemies has been highly destructive of El Salvador by UC scientists. Colonized Special close-up photography by Jack K.

C. utilis implanting an egg into its host. 80 times lifesize

Left, normal walnut aphid nymph right mummified nymph containing Parasitized olive scale [Parlaloria oleae (Colvee)] showing small holes a developing T. pallidus. where adult wasps have emerged after development within the scale host.

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