Classical biological control of brown citrus aphid: release of Lipolexis scutellaris

By: Marjorie A. Hoy and Ru Nguyen

The brown citrus aphid (BCA), Toxoptera citricida, was first detected in Florida in November 1995 in Dade and Broward counties. The BCA now has spread throughout the citrus growing region of Florida and could, in future, spread to other citrus-growing regions in the USA. The brown citrus aphid is a pest of citrus in Asia, apparently preferring citrus species and a few closely- related Rutaceae as hosts. The BCA has a relatively simple life history. All individuals are parthenogenetic females, producing live young. A single female thus can initiate a colony, and populations can increase very rapidly. Nymphs mature in six to eight days at temperatures of 20ºC or higher, with a single aphid theoretically able to produce a population of 4,400 within three weeks if natural enemies are absent.

The brown citrus aphid causes economic losses both in groves and nurseries. Adults and nymphs feed on young citrus foliage, depleting the sap. Their feeding can destroy the growing tip of citrus shoots. They also produce honeydew, which allows the sooty mold to grow. More importantly, this aphid is able to transmit citrus tristeza virus (CTV) more efficiently than other aphid species found on citrus in Florida. Detailed knowledge of the mechanisms by which the BCA transmits CTV is lacking. CTV is a phloem- limited virus with mild and severe strains and is transmitted in a non-persistent manner by the BCA, meaning that if the aphid is removed from a CTV-infected plant, it can no longer transmit the virus after about 48 hours. CTV does not multiply in the aphid. CTV also is transmitted by mechanical inoculation and grafting.

Citrus propagated on sour orange rootstock is especially susceptible to CTV and at least 18 million citrus trees in Florida currently are propagated on such rootstock. Thus, replanting of substantial acreage will be necessary in the next few years. In addition, budwood must be maintained free of CTV because this virus is graft-transmissible. Another danger potentially facing Florida's citrus industry is the possibility that the BCA will transmit stem-pitting strains of CTV, which are more virulent than the CTV strains that cause citrus "decline". Stem pitting CTV can attack and kill trees on rootstock that is tolerant of the milder decline strains.

Natural Enemies of the BCA

By the time the BCA was detected in Florida, it had spread through a sufficiently large area that it was not amenable to eradication efforts. Natural enemies of the BCA already present in Florida include parasitoids, predators, and pathogens-- especially fungi. It is likely that the native fungi assist in suppressing the BCA in Florida during the summer rainy season. Several predators, including ladybird beetles and syrphid fly larvae, and two parasitoid species also attack the BCA in Florida, but populations of the BCA still can increase dramatically during spring and fall. These population increases could be due, in part, to the fact that the most common parasitoid attacking the BCA in Florida is relatively ineffective. Lysiphlebus testaceipes attacks the BCA, but it rarely develops successfully in it so is unable to multiply when only the BCA is present. Another parasitoid, Aphelinus gossypii, which was introduced into Florida from Hong Kong in 1963 for control of spiraea aphid, Aphis spiraecola, has been recovered from the BCA but more commonly attacks other aphids.

Release of Lipolexis scutellaris

Lipolexis scutellaris Mackauer (Hymenoptera: Aphidiidae) is able to attack the BCA and successfully develop in it. L. scutellaris is widely distributed throughout Asia, where it is known to attack the BCA and several other aphid species in citrus. The establishment of L. scutellaris in Florida thus has the potential to reduce BCA populations in groves and dooryard citrus and may slow the transmission of CTV.

Adults of L. scutellaris were imported into quarantine facilities in Gainesville, Florida from Guam on August 19,1999. An application to release L. scutellaris was submitted to the Division of Plant Industry and permission to release L. scutellaris was given on June 21, 2000. The first releases took place on June 27, 2000 in Gainesville. Additional releases will be made throughout Florida's citrus growing region during 2000 and 2001.

L. scutellaris will be released throughout the citrus-growing area in Florida. Releases of 100 to 200 adults per release site are planned so that this natural enemy can be widely distributed. Citrus groves will serve as release sites if the owner agrees to eliminate toxic pesticides for one year, allow researchers back into the orchard to monitor establishment of the parasitoids, and provide approximately 1 to 2 acres for this purpose so that a 'buffer zone' is present to reduce potential mortality by toxic pesticide spray drift from adjacent citrus trees. Based on information obtained regarding toxicity of pesticides to the citrus leafminer parasitoid Ageniaspis citricola, we expect that citrus growers could safely apply oil and copper for pest and disease control in the release sites. The most favorable release sites in citrus groves will be where trees of mixed ages are present so that flushes are frequent, which helps to maintain aphid populations in the grove.

Biology of Lipolexis scutellaris

L. scutellaris is an endoparasitoid with four larval instars. Females deposit an egg within the aphid, the egg hatches and the larva consumes the internal organs of the aphid. Before completing its development, the parasitoid larva spins a cocoon inside the empty aphid exoskeleton, turning the aphid exoskeleton into a 'mummy'. The parasitoid pupa develops within the mummy and the small adult wasp emerges through a circular hole. Newly emerged adults need a short time to mature before mating, which lasts several seconds. Mated L. scutellaris females produce both female and male progeny but unmated females produce only males. Development usually takes about 12-13 days at 79ºF. Although parasitism ultimately results in mummification and death, parasitized aphids can feed and develop for some time. L. scutellaris is the primary parasitoid of the BCA in Guam and Dr. Ross Miller noted that L. scutellaris has established itself as the major parasitoid of aphids on Guam's citrus and vegetable crops. On Guam this parasitoid attacks the BCA, the melon aphid (Aphis gossypii), the cowpea aphid (Aphis craccivora) and the spirea aphid (Aphis spiraecola), all of which are found on citrus in Florida. On Guam, L. scutellaris most commonly is found parasitizing the BCA on tangerine, lemon, calamondin and orange, and parasitizing the melon aphid on cucumber, eggplant, melon and squash (Ross Miller, personal communication). L. scutellaris females are capable of depositing approximately 200-300 eggs. Observations in the Gainesville quarantine facilities indicate that females prefer to deposit eggs within small aphids. L. scutellaris has a relatively short generation time (ca. 12-14 days at 75-79ºF in our quarantine facility). Interestingly, L. scutellaris mummies are found in the soil under the potted citrus trees in quarantine rather than on the foliage; in some aphid species this behavior is correlated with very high aphid densities, which is certainly true in our quarantine rearing facility. This dispersal behavior by the parasitized aphids may make it difficult to monitor parasitism by L. scutellaris in the field. This behavior also raises concern as to whether the imported red fire ant, or other ants, will attack and kill these mummies when they are in the soil of Florida's citrus groves. It is possible that the mummies will not be attacked, because some ant species have been observed defending aphid mummies, which could enhance the likelihood the parasitoid is able to emerge.

L. scutellaris is widely distributed in India, Pakistan, southern China, Taiwan, Vietnam, and Japan, and some biological control scientists believe that L. scutellaris' ability to parasitize aphids other than the BCA should be helpful in obtaining establishment and in ensuring its effectiveness because the other aphids can serve as hosts when BCA populations are low.

Risk Assessment

Classical biological control programs are reviewed to determine potential risks, such as the impact of the natural enemy on nontarget species. Dr. Jim Cuda (personal communication, Department of Entomology and Nematology, UF, Gainesville) does not expect L. scutellaris to interfere with any weed biological control program because aphids are rarely used as natural enemies in weed control programs.

The risk of negative effects on nontarget aphids should be low. Dr. Susan Halbert, an expert on aphids at the Division of Plant Industry, Florida Department of Agriculture and Consumer Services in Gainesville, responded to questions as to whether L. scutellaris "...might attack nontarget aphids and if so, whether the environmental consequences would be serious enough to abandon plans for release." She concluded that "... exotic aphid parasites are not likely to have much negative effect on Florida's ecosystems. Aphids are obligate plant parasites. Without their host plants, they die. In my opinion, the only way to endanger an aphid species is to endanger its host plant. Although non-specific aphid parasites may attack native aphids, they are more likely to attack the relatively abundant pests of commercial and ornamental crops. Aphids are the ultimate r-strategists. Many species are capable of a 1000 fold increase in a 3-week time period. Populations of aphids fluctuate markedly throughout the year under natural conditions and are unlikely to be affected much by a new parasite unless it selectively attacked them at low density. It is improbable that an exotic general parasite would selectively attack an obscure native aphid at low density."

Based on our current knowledge of the biology of the Guam biotype of L. scutellaris, its expected geographic range is where the BCA becomes established in citrus in the USA. If the BCA spreads to other citrus-growing regions, L. scutellaris could move with the BCA into Louisiana, Texas, Arizona, and California. Because the Guam biotype could have a host range that includes melon aphid, cowpea aphid and spirea aphid, all of which are found on citrus in Florida, the Guam biotype of L. scutellaris could be found where these aphids are found, which could include host plants in addition to citrus. Because L. scutellaris is from a tropical/subtropical climate, we do not expect it to colonize temperate regions.

L. scutellaris is expected to establish on the BCA and to reduce BCA populations. Reductions in the use of pesticides to control this pest could result, leading to fewer negative effects on a variety of natural enemy species in citrus, or negative effects on the ground water, workers, or consumers.

Acknowledgments

We obtained adults of L. scutellaris from Guam courtesy of Dr. Ross Miller. We thank Shane Hill, Larry Keal, Scot Waring and Bob Weston for assistance in rearing L. scutellaris. Dr. Petr Stary confirmed the identity of the parasitoids and Dr. Susan Halbert provided useful advice on preparing the application to release L. scutellaris. John Capinera and Connie Riherd provided a review of the manuscript.

Hoy is in the University of Florida's Department of Entomology and Nematology at Gainesville; Nguyen is in the Florida Department of Agriculture and Consumer Services' Division of Plant Industry in Gainesville.

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