The Opportunistic Origin of a New Citrus Pest

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The Opportunistic Origin of a New Citrus Pest Left photo: Anise swallowtail larvae undergo dramatic color changes as they grow. The very small larvae are thought to mimic a bird dropping. Right: Young anise swallowtail larvae eat only tender leaves, but larger larvae can also damage mature citrus foliage. Arthur M. Shapiro 0 Kenneth K. Masuda wheredo new pests come from? Usual- of the carrot family. In California it occurs of a strain. We believe that natural selection ly, somewhere else. But every once in a from sea level to above tree line. Over so accomplished the same thing on sweet fen- while a native species that had been consid- wide a range, its life history is quite vari- nel in the field. The advantages of multiple- ered innocuous is “suddenly” tranformed able. In the bleak high mountain meadows broodedness are obvious; a shorter genera- into an enemy of agriculture. The classic it has only one generation during the short tion time means leaving more descendants example is the Colorado potato beetle, growing season. At sea level it may have per unit time. Where summer hosts are not which moved from weedy wild nightshades four or five per year; it flies from March to available, selection would constantly weed onto the related cultivated potato and October or November in the Sacramento out any deviant animals that failed to enter marched from potato field to potato field Valley, and all year round in coastal San dormancy. In the high Sierra, encroaching across the continent. Diego County. cold weather would arrest development Why should an insect move onto a new Yet this continuous breeding was appar- anyway, and in years of light snow pack a host? The answer is frequently chemical. ently impossible before the white man came partial second generation can occur. Sims Most insects are specialists on particular to California: all the native lowland host found that foothill, serpentine populations kinds of plants, which they recognize by plants dry up during the long, rainless sum- were the most obstinately single-brooded, means of distinctive chemical compounds mers. Once sweet fennel was introduced by whereas a population from 7,000 feet (Don- peculiar to those plants. They also avoid the Spaniards in the 18th century, the swal- ner Pass) was intermediate, and Central plants containing repellent chemical stimu- lowtail could rear generation after genera- Valley populations were strongly multiple- li, even if the proper attractants are also tion in warm weather. As the plant spread brooded under lab rearing regimes. present. If man introduces a new plant in an to every vacant lot in the valleys, the butter- Orange (Citrus sinensis) belongs to the area, and it is stimulatory but not repellent fly followed it, so that by the second half of rue family (Rutaceae). Like fennel, it was to an insect already there, a new pest may the 19th century the multiple-brooded introduced to California by the Spaniards. be born. Only about ten years ago such a insect was generally distributed in agricul- Commercial orange groves began near Los process began to operate in citrus groves in tural and urbanized California. Angeles by 1841. By 1975 225,000 acres the northern Sacramento Valley; for the When we examine the physiology of these were in citrus production in California and first time growers had to pay attention to a multiple-brooded zelicaon, it is clear that Arizona. The anise swallowtail was not re- pretty yellow and black butterfly named they differ profoundly from the single- ported on citrus until about 1918. In 1922 Papilio zelicaon. brooded populations that still exist at low J. R. Horton published a 10-page paper in In California Papilio zelicaon is usually elevations in wild parts of the state where the Monthly Bulletin on P. zelicaon as a called the anise swallowtail, reflecting its sweet fennel does not grow. In fact, there citrus pest near Visalia. It has been a pest in most common host plant; “anise” in Cali- are physiological races, which we have southern California ever since, but it re- fornia usually refers to sweet fennel, Foeni- shown in the lab to differ genetically in their mained unknown as such in the citrus- culum vulgare, an abundant perennial weed propensity to enter and terminate dormancy. growing areas near Chico for another 45 of the carrot family (Umbelliferae). The Single-brooded races persist particularly on years or more. story of P. zelicaon, sweet fennel, and serpentine soils and can sometimes be found In retrospect, the swallowtail’s move citrus growing is best told historically, as we close to multiple-brooded, fennel-feeding onto citrus is hardly surprising. In the genus have been able to reconstruct it. ones at the same elevation. Papilio we find rue feeders, umbellifer Papilio zelicaon is apparently a native Dr. Steven R. Sims, working in our lab at feeders, and species that move back and insect, found throughout western North Davis, found that artificial selection can forth between these (not closely related) America, feeding on various wild members rapidly alter the dormancy characteristics plant families. A swallowtail is a major 4 CALIFORNIA AGRICULTURE, JUNE 1980 citrus pest in South Africa. Another, the kins Host-Selection Principle” did not orange dog (P. cresphontes), long common hold. in the southeast, has expanded its range Evolution of a citrus race was still pos- from Arizona into southern California. As sible if citrus were intrinsically a better host early as 1941, Vincent G. Dethier, working than sweet fennel; we therefore compared with another swallowtail (P. polyxenes of growth, survivorship, and fecundity of the eastern United States, a close relative of both strains on both plants. Once again, we P. zelicaon), showed that the rue and citrus found fennel was intrinsically superior to families shared essential oils (anethole, citrus on all counts. The female lays her methyl chavicol, anisic aldehyde, and the eggs on the young, growing shoot tips of like) that were feeding stimuli to the insect: citrus; young caterpillars can eat only caterpillars will eat filter paper treated with tender, young leaves, although larger ones them, but won’t eat umbellifer foliage that can handle mature foliage. This limits pop- lacks them. The chemistry provided a ulation levels, focuses the damage, and natural “bridge” to a new host plant. makes citrus trees a trickier host than fen- We believe that P. zelicaon has crossed nel, all parts of which are available all year. that chemical bridge at least twice-once in Why, then, is the anise swallowtail at- the south and a second time, more recently, tacking citrus at all? The answer seems to be in the north. (This is to be studied further straightforward: it has nothing to lose. by genetic analysis of crosses between the There is no fennel in the vicinity of the northern and southern citrus-feeding popu- orange groves. By using citrus, the butterfly lations and crosses of both with tester has expanded its range into areas it could stocks.) We wondered why, and whether it not occupy before. There is nothing wrong Spring planting is best was evolving a citrus race just as it had with using a suboptimal host if that is the evolved a sweet fennel race. only host around. Sweet fennel is highly attractive to fe- Right now the U.C. recommendations for oilseed sunflower males from populations feeding on wild for swallowtail control on citrus are Para- umbellifers. Sims also found in split-brood thion, Phosdrin (mevinphos), or Guthion Benjamin H. Beard 0 Karl H. lngebretsen experiments that the insect has a lower pro- (azinphosmethyl). All are highly toxic, pensity to dormancy when fed on fennel deadly to honey bees and beneficial para- than on short-lived plants, even in the sites, and subject to many restrictions. The multiple-brooded strains. The shift onto ecology of the situation suggested the pos- Non-oil (confectionery) sunflowers (Heli- fennel over a century ago might have been sibility of trap-cropping with sweet fennel anthus annuus L.) have been grown in the aided by the “Hopkins Host-Selection where the swallowtail becomes a significant Sacramento Delta of California since the Principle” proposed by A. D. Hopkins in problem. We carried out field tests with early 1930s. Production has varied from 1917, which holds that given a choice potted plants in citrus orchards, which about 800 to 3,200 hectares (2,000 to 8,000 among acceptable hosts, a female insect will showed the same female preference for fen- acres) per year with yields of 1,100 to 3,900 prefer to lay eggs on the one she herself ate. nel as had been found in the lab. kilograms per hectare (1,OOO to 3,500 Once the species had made an initial break- Because fennel regenerates quickly from pounds per acre). The larger seeds are used through, the developmental-time advan- its taproot, strips of it interplanted with for direct human consumption, and the tages would assure a rapid spread of fennel citrus could be mowed regularly, after the small seeds are fed to birds. The oil content preferences in the population. James Erick- egg-laying peak in each generation. We of the whole seed ranges from 25 to 30 per- son found in research at Cornell that this have found that regenerating sweet fennel is cent. “larval memory ” occurred in Papiliopoly- more attractive to females than uncut tops. In the 1940s an oil-type sunflower with xenes, but Christer Wiklund, working on a Sweet fennel flowers are visited by many seeds containing 30 to 35 percent oil was in- Swedish species of the same group, found it dipteran and hymenopteran natural troduced into the United States.
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