Biology and Control of Brown Citrus Aphid (Toxoptera citricida Kirkaldy) and Citrus Tristeza

James H. Tsai, Ying-hong Liu 
Fort Lauderdale Research and Education Center, IFAS
University of Florida
3205 College Avenue, Ft. Lauderdale, FL 33314

Richard F. Lee
Citrus Research and Education Center, IFAS
University of Florida
700 Experiment Station Road, Lake Alfred, FL 33850

C. L. Niblett
Department of Plant Pathology, IFAS
University of Florida
Gainesville, FL 32611

Citrus is one of the most important crops in Florida, California, Texas and Arizona. It is not only important economically in term of foreign trades and employment opportunities, but it also contributes significantly to human nutrition. In Florida alone, the annual value of citrus is estimated at $1.1 billion, and the overall value of citrus at the national level was over $8 billion in 1996. There are 857,687 acres planted in citrus with a total of 107 million trees in the 33 citrus producing counties. Florida is the leading producer of all citrus in the U.S., amounting to more than 70% the national production. Like many other crops citrus has many pest and disease problems; among them the efficient aphid vector of citrus tristeza virus (CTV), commonly called the brown citrus aphid (BrCA), Toxoptera citricida Kirkaldy. Since the BrCA was first discovered in south Florida in November, 1995, this aphid has posed a real and serious threat to the citrus industry. Not only does BrCA damage citrus directly through feeding, but most importantly it transmits efficiently the severe strains of CTV. Disastrous epidemics of CTV have occurred in Argentina, Brazil, Colombia and Peru (Rocha-Pena et al. 1995). In view of the vast interest in this pest, this chapter attempts to synthesize the information on the biology and ecology and management of BrCA as well as its transmission of CTV.

Geographical Distribution of BrCA:

The origin of BrCA is thought to be in Southeast Asia (Kirkaldy 1907; Rocha-Pena et al. 1995). It has been reported in the Pacific region including China, Taiwan, India, Japan, Laos, the Philippines, Viet Nam, Thailand, Nepal, Indonesia, Malaysia, Sri Lanka, Hawaii, Fiji, Mauritius, Reunion, Samoa, Tonga, Australia and New Zealand (Essig 1949; Carver et al. 1994; Cottier 1935; Banziger 1977; Hely 1968; Gavarra and Eastop 1976; Laing 1927; Lever 1940; Kirkaldy 1907; Knorr and Moin Shah 1971; Mamet 1939; Moreira 1967; Takahashi 1926; Van Der Goot 1918). Brown citrus aphid has also been recorded in Africa including Cameroon, Congo, Ethiopia, Ghana, Kenya, Morocco, Mozambique, Somalia, South Africa, Tanzania, Tunisia, Uganda, Zaire, and Zimbabwe (Essig 1949; Abate 1988; Annecke 1963; Theobald 1928; Halima et al. 1994). BrCA is found in the western hemisphere: Argentina, Belize, Brazil, Bolivia, Chile, Colombia, Costa Rica, Cuba, Dominica, Dominican Republic, El Salvador, Florida in the USA, Guadeloupe, Guyana, Haiti, Jamaica, Martinique, Nicaragua, Peru, Puerto Rico, St. Lucia, Surinam, Trinidad, Uruguay, and Venezuela. (Aubert et al. 1992; Bisessar 1968; Geraud 1976; Halbert and Brown 1996; Lastra et al. 1991 and 1992; Rocha-Pena et al. 1995; Roistacher 1988; Squire 1972; Yokomi et al. 1994; van Hoof 1961).

Host Range of BrCA:

The reports on the association of BrCA with many species of Anacardiaceae, Bombaceae, Bureraceae, Camelliaceae, Caryophyllaceae, Dioscuraceae, Ebenaceae, Ericaceae, Euphorbiaceae, Fagaceae, Flacouatiaceae, Juglandaceae, Leguminoceae, Lauraceae, Malpighiaceae, Malvaceae, Moraceae, Mysinaceae, Nyctaginaceae, Oxalidaceae, Passifloraceae, Rosaceae, Robiaceae, Rutaceae, Ternstroemiaceae, Ulmaceae and Urticaceae have recently been reviewed and summarized by Michand (1998). Most researchers generally agree that collections or observations of BrCA from the non-rutaceous plant species do not necessarily mean these are suitable for development and reproduction for BrCA unless a host suitability study has been conducted to support the fact. For example, the tender shoots of Ficus retusa var. nitida (Thumb) Miq. had often been observed to be colonized by BrCA in citrus grove in South Florida; however, many attempts were made to rear this insect on this host in the laboratory to no avail (Tsai 1998). Many observations of BrCA being associated with non-rutaceous plants could be attributable to misidentifications (Stoetzel 1994).

Bionomics of BrCA:

BrCA was first described as a member of genus Myzus by Kirkaldy in 1907. Since then the scientific name of BrCA has undergone several changes (Denmark 1978; Stoetzel 1994).

Biology studies conducted under field conditions showed that the BrCA development time was 8--21 days, and there were about 30 generations per year in southern Rhodesia (Symes 1924). Like other aphids, BrCA normally does not reproduce sexual adults, except under temperate conditions in Japan (Komazaki et al. 1979). A recent detailed study on the biology and life history of the BrCA showed that the host plants significantly affected development, survival longevity and reproduction of BrCA (Tsai 1998). Immature survival at 25 ± 1° C on sour orange, C. aurantium L.; grapefruit, C. paradisi Macfadyen; key lime, C. aurantifolia Swing; calamondin, X Citrofortunella microcarpa (Bunge) Wijnands; rough lemon, Citrus jambhiri Lush.; orange jassamine, Murraya paniculata (L.) Jack; box orange, Severinia buxifolia (Poir) Tenore; lime berry, Triphasia trifolia (Burm. f.) P. Wilson were 93.5, 93.3, 88.3, 86.5, 82.0, 62.8, 53.1, and 41.6%, respectively. Developmental times for the immature stages among populations on rough lemon, sour orange, grapefruit, and key lime were 5.9--6.2 days. Longer development periods (6.5--7.2 days) occurred on box orange, calamondin, lime berry, and orange jassamine. The average number of nymphs reproduced per female were 58.8, 43.0, 42.5, 34.1, 32.7, 17.7, 20.8 and 23.0 on sour orange, grapefruit, rough lemon, key lime, calamondin, box orange, lime berry, and orange jassamine, respectively. Female adults lived an average of 22.1, 19.5, 18.0,17.5, 22.8, 16.3, 22.6, and 14.6 days on these same hosts. The intrinsic rate of natural increase (rm) for BrCA on grapefruit was highest. Jackknife estimates of rm varied from 0.381 on grapefruit to 0.183 on lime berry. The mean population generation time on these hosts ranged from 9.7 to 12.2 days. This study showed that these hosts could support BrCA populations when the new flushes are not available in commercial citrus groves (Tsai 1998). Komazaki (1982) also noted that BrCA reared on C. aurantium at 25.1° C had a much lower net reproductive rate (36.8) and longer mean generation time (11.3 days) than those reared on C. unshiu.

The environmental factors, especially temperature, has a great effect on the biology and life history of BrCA. Takanashi (1989) studied the reproductive rates of alate and apterous adults of BrCA at 20° and 25° C reared on C. natsudaidai and found that age-specific fecundity and net reproductive rate of apterae were higher at both tempertures. Komazaki (1982) reported that the intrinsic rate of increase for BrCA was highest at 27° C., although the maximum facundity and net reproductive rate of individual adults were at 21.5° C. A recent temperature study conducted by Tsai and Wang (1999) showed that BrCA is sensitive to temperature. The development, survivorship, and reproduction of BrCA were evaluated at 8 constant temperatures (8, 10, 15, 20, 25, 28, 30 and 32° C). The developmental periods of immature stages ranged from 63.1 days at 8° C to 5.5 days at 30° C. The lower developmental threshold for the immature BrCA was estimated at 6.27° C. The upper temperature threshold of 31.17° C for development of nymphs was determined from a nonlinear biophysical model. The survivorship percentage of immature stages varied from 81 to 97% within the temperature range of 8--30° C. However, survivorship was reduced to 29% at 32° C. The average longevity of adult females ranged from 60.0 days at 10° C to 6.5 days at 32° C. The average number of progeny per female was 52.5 at 20° C and 7.5 at 32° C. The largest rm (0.3765) occurred at 28° C. Populations reared at 10 and 32° C had the smallest rm values of 0.0588 and 0.0960, respectively. The mean generation time of the population ranged from 51 days at 10° C to 8 days at 32° C. The optimal range of temperature for BrCA population growth was 20--30° C. Several mathematical functions were used to quantify BrCA development, survivorship, reproduction and lifetable parameters in relation to temperatures (Tsai and Wang 1999).

Responses to extreme low temperatures vary considerably among aphid species and even among different colonies for biotypes of same species. The developmental threshold of 6.27° C for the BrCA nymph in Florida is lower than the threshold of 7.4° C reported for summer generation BrCA reared at fluctuating temperatures (Komazaki 1988). Nickel and Klingauf (1985) reported that extreme temperatures in winter and summer had a negative impact on BrCA development.

The intrinsic rate of natural increase is a good indicator of the temperature at which the growth of population is most favorable because it reflects the overall effects of temperature on development, reproduction, and survival characteristics of a population. Brown citrus aphid reared at 28° C had the highest rm value (0.3765) among all temperatures, because of its faster development, higher survivorship of immature stage, and higher total progeny production, as well as its considerably higher daily rate of progeny production. The net reproductive rates of 33.13, 44.32, and 41.08 at 15, 20, and 25° C, respectively, recorded for the Florida colony of BrCA are generally higher than the 44.3, 38.84, and 35.79 at 15.2, 19.9., and 24.9° C previously reported for BrCA reared on C. aurantium in Japan (Komazaki 1982). Likewise, the mean generation times at these three temperatures are also shorter than those reported by Komazaki (1982). These differences could be the result of different species of host plant or biotypes of the insect. The development-rate model derived from constant temperature data (Tsai and Wang 1999) can be used to estimate developmental time of these aphids under natural conditions of temperature varying within an appropriate range (Kaufmann 1932).

Field Populations:

There have been numerous reports of outbreaks of BrCA on the new flushes of citrus following heavy rainfall (Schwarz 1965; Klas 1979). In areas such as Argentina, Australia, Brazil, Kenya, Taiwan and Japan, generally two distinct population peaks per year were observed; one each in the spring and fall seasons (Nickel and Klingauf 1985; Khan 1976; Chagas et al. 1982; Seif and Islam 1988; Tao and Tan 1961, Nakao 1968). A field survey was conducted in a citrus grove in South Florida from March 1996 to October 1998. The results of weekly samplings of 60--80 trees showed that there were two major peaks of BrCA populations per year. However, the peaks did not fall on the same months each year. They were solely dependent on the rainfall of preceding month (Tsai, unpublished).

CTV Strains, Strain Variation and Symptomatology:

CTV is a member of the closterovirus group (species Citrus tristeza virus; genus Closterovirus; family Closteroviridae) and is considered one of the most economically important virus pathogen of citrus (Bar-Joseph et al, 1989, Bar-Joseph et al, 1992). Disastrous epidemics of CTV have occurred in Argentina, Brazil, and Venezuela following the introduction of the BrCA (Roch-Pena 1995). The most important CTV strains are quick decline on sour rootstock and stem-pitting on susceptible scions (Lee et al, 1994). For many years, researchers have been handicapped for lack of a quick and reliable assay technique to detect different CTV strains in single and mixed infections. This, plus the fact that the virus in phloem-limited, extremely long and flexuous, limited to perennial hosts and in low concentrations, our understanding of this virus has been slow to develop.

CTV exists as a complex of many strains which cause diverse symptoms (Rocha-pena et al, 1995). CTV strains fit into one or more of the following broad categories: mild strains (causing no discernable effect on commercial citrus); decline on sour orange rootstock strains (cause decline and death of trees on sour orange rootstock); seedling yellows strains (cause dwarfing and chlorosis in grapefruit and sour orange); and stem pitting strains. The stem pitting strains may produce stem pitting on either sweet orange cultivars and/or grapefruit cultivars. In some area, CTV strains are found which cause stem pitting on rootstocks normally considered to be "CTV tolerant", examples are the Capao Bonito strain in Brazil which affects Rangpur lime rootstock, strains in South Africa which stem pit rough lemon, and strains in Venezuela which stem pit rough lemon, volkamer lemon, and even Cleopatra Mandarin (Rocha-Pena et al, 1995). The severity of symptoms expressed by the different strains can be from mild to very severe. The decline on sour orange strains of CTV are important when sour orange is the prinicipal rootstock being used. The stem pitting strains of CTV are important economically because of decreased tree vigor, twig dieback and canopy thinning, and a reduction in fruit set, fruit size and quality. Stem pitting on grapefruit can reduce yield by up to 45 percent (Marais). Control of stem pitting strains of CTV is difficult because they affect either the scion and/or rootstock, and control is not as simple as just to use "CTV tolerant" rootstocks as can be done to prevent future losses to the decline on sour orange strains. The biological properties of a specific isolate of CTV (which is usually a mixture of several strains) is determined by indexing on a battery of indicator plants (Garnsey et al, 1987). This evaluation of biological activity takes about one year under ideal greenhouse conditions. Some progress has been made recently of laboratory diagnostic procedures to differentiate CTV strains on a more timely basis (Lee et al, 1997, Rocha-Pena and Lee, 1991), but additional field verification of these methods is needed.

Each CTV strain varies in its vector transmissibility (Roch-Pena et al. 1995). CTV is easily graft transmissible as long as phloem tissue from the inoculum is in contact with the phloem of the receptor plant (Rocha-Pena et al, 1991). Movement of nursery materials which have been propagated from a CTV-infected budsource is the mechanism of most long distance movement of the virus. The virus and can be mechanically transmitted with partially purified inoculum by slash inoculation (Garnsey and Muller 1988).

CTV Transmission by BrCA:

CTV is transmitted semi-persistently by Aphis gossypii Glover, A. spiraecola Patch, A. craccivora Koch, Dactynotus jacae L., Toxoptera aurantii Boyer de Fonscolombe, and T. citricida (Bar-Joseph and Lee 1989; Rocha-Pena 1995; Roistacher and Bar-Joseph 1987). Different strains vary greatly in aphid transmissibility (Rocha-Pena, 1995). BrCA is the most efficient vector of CTV followed by A. gossypii. The relative single aphid transmission efficiencies by these two aphids from side by side tests were 16.0 and 1.4% (Yokomi et al. 1994). The transmission efficiency of A. spiraecola at least three times less than that of A. gossiypii, but A. spiraecola is the most abundant citrus aphid in the U.S (Yokomi and Garnssey 1987). Although A. gossypii is less efficient at CTV transmission than the BrCA, it has efficiently transmited decline and stem-pitting strains of CTV in Isreal, California and Florida (Bar-Joseph and Loebenstein 1973; Roistacher 1981; Yokomi and Garnsey 1987).

Beginning in 1997, a series of CTV transmission trials using single aphid transmission tests with the BrCA have been conducted. Serological assay of about 2500 test plants singly inoculated by BrCA with mild and severe strains of CTV indicated that transmission rates ranged from 1 to 13% after a 24--48 hour acquisition access period (Tsai, Lee and Niblett unpublished).

Control Measures:

The effective control of the BrCA/CTV disease complex requires an integrated pest management approach. The individual components are discussed here.

A. Biological Control Agents:

A number of natural enemies have been observed to attack BrCA in South Florida. They include lady beetles Coelophora inaequalis (Fab.); Cycloneda sanguinea sanguinea (L.); parasitic wasps (Lysiphlebus testaceipes (Cresson); Aphelinus gossypii (Timberlake); a syrphid, possibly Pseudodorus clavatus (Wiedmann); and unidentified lacewings; as well as fungal entomopathogens.

A preliminary study of C. inaequalis development in South Florida indicated that average development times at 25° C for egg, 1st instar, 2nd instar, 3rd instar, 4th instar, prepupa, and pupa were 3.00 ± 0.0, 1.42 ± 0.5, 1.41 ± 0.5, 1.82 ± 0.40, 3.33 ± 0.49, 1.10 ± 0.50, and 3.30 ± 0.67 days, respectively. Average adult longevity was 104.6 ± 13.4 days, and mean number of eggs laid by female per life was 687.8 ± 125. The average daily number of BrCA nymphs consumed by adult lady beetle were 44 ± 2.5 and mean daily number of BrCA adults consumed by this predator were 23.6 ± 4.3. This predator preferred BrCA nymphs to adults (Tsai, unpublished). This predator appeared to suffer no toxic effect from aphid food source as described by Tao and Chiu (1971).

Lysiphlebus testaceipes has often been observed to parasitize BrCA in south Florida especially when the BrCA population is high (Tsai, unpublished). The role of this native parasitoid plays in suppression of BrCA is currently under investigation.

A parasitoid, Lysiphlebia japonica(Ashmead), was imported from Japan in 1996. The bionomics of L. japonicawas studied at five constant temperatures (10, 15, 20, 25 and 30° C) using BrCA as rearing host (Deng and Tsai 1998). Developmental rate from oviposition to emergence of adult wasps increased linearly with increasing temperature between 10--25° C. Developmental periods from oviposition to adult wasp emergence ranged from 29.7 days at 10° C to 9.9 days at 25° C. Developmental threshold and degree day (DD) requirement for development from oviposition to adult eclosion were 2.9° C and 223.46 DD. The percentage of parasitized aphid varied from 49.93--23.47% within the temperature range of 10--30° C. Pupal survivorship and sex ratio decreased as temperature increased between 10--30° C. Based on our data, this parasitoid is presumably more effective in control of BrCA in cooler months than in summer. Over 11,000 L. japonica were released during the 1996-1997 seasons in citrus groves in South Florida. The initial recovery of this parasitoid was only successful in the cool months (January and March) (Deng and Tsai 1998).

Other such biocontrol agents as hyphomycete insect pathogenic fungi were also investigated in South Florida (Poprawski et al. 1999). Single- and multiple-dose bioassays and field trials were conducted to evaluate the efficacy of various isolates of entomopathogenic fungi against the BrCA . Single-dose bioassays demonstrated that BrCA is susceptible to several isolates of Beauveria bassiana (Balsamo) Vuillemin, Paecilomyces fumosoroseus (Wize) Brown & Smith, and Metarhizium anisopliae (Metschnikoff) Sorokin. Overt mycosis ranged from 23.1% (M. anisopliae ARSEF 759) to 78.0% (B. bassiana SARC 6000). In multiple-dose bioasssays, good dose response was obtained with 3 B. bassiana isolates. The 6-day LD50 values for these isolates ranged from 119 to 995 conidia per square millimeter. There was a strong correlation (slopes>1.30) between rapid rise in mortality and dosage increase for all 3 isolates. Replicated field trials of the B. bassiana (strain GHA)-based mycoinsecticide Mycotrolâ ES provided relatively rapid kill at the application rates. The 5-day Abbott percent efficacies of Mycotrol ES were, respectively, 79.8 and 94.4% at the half and full rates (2.5 x 1013 and 5 x 1013 conidia/ha). Proportions of overt mycosis ranged from 0.67 at the half rate to 0.80 at full rate. Mycotrol ES could be an important component of integrated BrCA management in the future (Poprawski et al. 1999).

B. Chemical Control:

Several reports of successful chemical control of BrCA are available (Hall 1930; Koli et al. 1978; Tao and Tan 1961; Tao and Wu 1968 and 1969; Portillo 1977;Yokomi et al. 1995). In Florida, two systemic insecticides Admire 2F (imidacloprid), and Temik (aldicarb) are currently registered for use on citrus. Our experiment showed that the average BrCA mortality from 15 potted citrus plants drenched with Admire (formulated product) at 32.5 ml/pot was 88.8% three months posttreatment. Another experiment was conducted to evaluate the efficacy of Temik 15G (formulated product) against BrCA in potted citrus plants in screenhouses and field grown citrus plants. An average of 83.17% of BrCA mortality was recorded from 15 potted plants treated with 62 gr of Temik six months posttreatment. Even when the dosage was reduced to 15 gr/pot, the average BrCA mortality from 15 potted plants was still 92.93% five months posttreatment (Tsai unpublished).

In replicated field trials, the average mortalities of BrCA feeding on grapefruit trees treated with 120g/tree Temik were 85.6 and 1.7% at 41 days and 104 days posttreatment, respectively. In similar trials with the same concentration of Temik, the average BrCA mortalities feeding on navel orange trees were 100, 86.4, and 3.3%, at 20, 48 and 82 days posttreatment, respectively (Tsai unpublished).

C. Virus resistance:

Poncirus trifoliata (L.) and some citranges and citrumelos which are hybrids of P. trifoliata are immune to CTV infection, e.g. no viral replication (Rocha-Pena et al,1995). Laboratories in Florida and California are mapping the immunity gene with the hopes of inserting this gene into desirable citrus cultivars using molecular techniques and, thus, produce CTV immune citrus (F Gmitter, personal communication; M. Roose personal communication). However a recent report indicates that strains of CTV may be present in New Zealand which break this source of resistance to CTV (Dawson & Mooney, 1998). Many Citrus species are known to be tolerate the CTV infection with no obvious symptoms of ill effect even though the virus replicates in these plants. Many commonly used rootstocks, such as Cleopatra mandarin, Rough lemon, Rangpur lime, Volkamer, are referred to as "CTV tolerant" because they are not affected by the decline on sour orange strains of CTV which kills trees on sour orange. These rootstocks are tolerant of CTV, e.g. the virus replicates, and some stem pitting strains of CTV can cause severe stem pitting in these rootstocks. Thus these CTV-tolerant rootstocks are useful in areas where stem-pitting strains which affect these rootstocks are not widespread.

Mild Strain Cross Protection:

Mild strain cross protection (MSCP) is the deliberate use of selected mild strains of a virus which when inoculated into a plant which is then challenged with a more severe strain of the same virus, suppresses the symptoms of the more severe strain of the virus (Lee et al, 1987 ). When discussing MSCP, it is important to realize that "mild" is a relative term in terms of virus severity (Lee et al, 1987, Lee et al, 1995). For example, the "Nartia" strain, which is used universally in South Africa to protect grapefruit from severe stem pitting, contains seedling yellows, produces some degree of leaf chlorosis, and causes mild stem pitting. If this "Nartia"strain were in Florida, it would be considered to be a very severe strain of CTV, but in South Africa, it is realitively "mild". In several citrus areas of the world, such as South Africa, Australia, Brazil, Reunion, India, and Japan, mild strains have been selected from outstanding trees which have performed well in the presence of endogenous severe CTV strains, and these mild strains are commercially used for MSCP. Because MSCP is strain specific, e.g. a certain mild strain will provide protection against specific severe strains, if new severe strains of CTV are introduced into the area, MSCP may not continue to provide protection. MSCP is also host specific; an isolate of CTV which gives protection in sweet orange will not necessarily protect grapefruit.

MSCP is not the same thing as virus resistance, rather it should be viewed as a way to extend the productive economic lifespan of a block of trees (Lee et al, 1995). Given continued challenge with severe strains, effects of stress such as freezes, extreme warm temperatures or drought, the protection ability will eventually be reduced. The ability of aphids to transmit either mild or severe CTV strains from mixed infections has been used as a criteria for preliminary selection of mild strains for cross protection (Yokomi et al, 1987).

D. Clean Stock/Certification Programs:

Being able to plant a healthy citrus tree, or a citrus tree which may have a preselected specific mild strain of CTV for MSCP, is a key component of the integrated pest management approach for the BrCA/CTV disease complex (Lee, Navarro and Lehman, 1998). The presence of other virus diseases, if present, severely limit the use of "CTV-tolerant" rootstocks. For example, viroids severe affects trees on P. trifoliata or hybrids which have P. trifoliata as one of the parents; woody gall severe affects trees on lemon-type rootstocks, such as rough lemon and Volkamer; cachexia severe affects trees on some mandarin-type rootstocks; citrus blight affects trees on most rootstocks except for sour orange, sweet orange and some citranges; citrus tatterleaf virus severely affects trees on P. trifoliata and hybrid rootstocks having P. trifoliata as one of the parents (Rocha-Pena et al. 1995). Thus, it is essential that budwood source trees come from a clean stock program, where the desired clones have been therapied for the elimination of virus and graft-transmissible agents, tested to verify the freedom from these pathogens, then maintained under protected conditions so that vector do not re-introduce the pathogens. Certification programs then allow for distribution of propagations of the healthy citrus to the growers, with a tracking system which allows for budwood sources to be traced should a problem occur once the tree is planted. Clean stock and certification programs also help ensure the citrus clones are horticulturally true-to-type.

F. Quarantine:

If a virus problem is not imported into a new area, the disease will not established and no further control is needed. Each citrus producing state in the U.S. has strict regulations regarding the movement of plant material and has a sound citrus budwood program in place. Success on these programs requires a high level of understanding and cooperation of growers and tourists as well as traveling public (Schoulties et al. 1987). Importation of new plant germplasm should be done only under quarantine conditions with therapy being used to eliminate any potential graft-transmissible pathogen, and through testing to ensure freedom of pathogens (Lee et al, 1998). The must be a way to legally, and safely, import new germplasm, otherwise the germplasm will enter illegally in shirt pockets and pose a potential threat to the industry if new pathogens are introduced with it.

D. Suppresion:

In some areas where CTV is not present, or present at a very low incidence, tree removal to reduce the inoculum can be useful. For example, the Central Valley in California has had a tristeza eradication program since 1957, and even now has less than one percent of the trees in the valley infected with CTV (Rocha-Pena, 1995). Eradication has been used in Israel to extend the useful life of sour orange as a rootstock (Bar-Joseph et al, 1989).


Appreciation is extended to the following for providing research funds: Office of Dean for Research, IFAS, FAES Research Program Enhancement Award, Florida Citrus Production Research Advisory Council and Rhone-Poulenc AG Company. This is Florida Agricultural Experiment Station Journal Series No. R-XXXX.


  • ABATE, T. 1988. The identity and bionomics of insect vectors of tristeza and greening diseases of citrus in Ethiopia. Trop. Pest. Man. 34: 19-23.
  • ANNECKE, D. P. 1963. Observations on some citrus pests in Mozambique and Southern Rhodesia. J. Entomol Soc. S. Afr. 26: 194-225.
  • AUBERT, B., J. ETIENNE, R. COTTIN, F. LECLANT, P. CAO VAN, C. VUILLAUME, C. JARAMILLO, AND G. GARBEAU. 1992. Citrus tristeza disease a new threat for the Caribbean basin. Reoprt of a survey to Colombia, Dominican Republic, Guadeloupe, Martinique and Trinidad. Fruits 47: 393-404.
  • BANZIGER, H. 1977. Keys to the identification of aphids (Homoptera). I. Winged aphids of species economically important in Thailand. F.A.O. Pl. Prot. Bull. 36: 2-41.
  • BAR-JOSEPH, M., AND R. F. LEE. 1989. Citrus tristeza virus. Description of Plant Viruses No. 353. Commonw. Mycol. Inst./Assoc. Appl. Biol. Kew, Surrey England.
  • BAR-JOSEPH, M. AND G. LOEBENSTEIN. 1973 Effects of strain, source plant, and temperature on the transmissibility of citrus tristeza virus by the melon aphid. Phytopathology. 63: 716-720.
  • BAR-JOSEPH, M., R. MARCUS, AND R. F. LEE. 1989. The continuing challenge of Citrus Tristeza Virus control. Ann. Rev. Phytopath. 27:291-316.
  • BISSESSAR, S. 1968. Citrus tristeza in Guyana. F.A.O. Pl. Prot. Bull. 16: 45-48.
  • CARVER, M., P. J. HART, AND P. W. WELLINGS. 1994. Aphids (Hemiptera: Aphididae) and associated biota from the Kingdom of Tonga, with respect to biological control. Pan-Pac. Entomol. 69: 250-260.
  • CHAGAS, E. F. D., S. S. NETO, A. J. B. P. BRAZ, C. P. B. MATEUS, AND I. P. COELHO. 1982. Population fluctuations of pest and predator insects in citrus. Pesqui. Agropecu. Bras. 17: 871-824. (in Port., Eng. sum.).
  • COTTIER, W. 1935. The black citrus aphid and some other tree aphides. N.Z.J. Agric. 51: 214-219.
  • DAWSON, T. AND P. MOONEY. 1998. Trifoliate resistance breaking strain of CTV in New Zealand. Pg 49 In: Abstracts of the 14th Conference of IOCV, September 13 - 18, 1998, Campinas, Brazil. IOCV, Riverside.
  • DENG, Y. X., AND J. H. TSAI. 1998. Development of Lysiphlebia japonica (Hymenoptera: Aphidiidae), a parasitoid of Toxoptera citricida (Homoptera: Aphididae) at five temperatures. Fla. Entomol. 81: 415-423.
  • DENMARK, H. A. 1978 The brown citrus aphid, Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Entomol. Circ. No. 194. Division of Plant Industry. Fla. Dept. Agric. and Cons. Ser.
  • ESSIG, E. O. 1949. Aphids in relation to quick decline and tristeza of citrus. Pan. Pac. Entomol. 25: 13-22.
  • GARNSEY, S. M., D. J. GUMPF, C. N. ROISTACHER, E. L. CIVEROLO, R. F. LEE, R. K. YOKOMI, AND M. BAR-JOSEPH. 1987. Toward a standardized evaluation of the biological properties of citrus tristeza virus. Phytophylactica 19:151-157.
  • GARNSEY, S. M., AND G. W. MULLER. 1988. Efficiency of mechanical transmission of citrus tristeza virus. P. 46-54 In L. W. Timmer, S. M. Garnsey, and L. Navarro, [eds.]. Proc. Conf. Intl. Org. Citrus Virol. 10th. Riverside, California.
  • GAVARRA, M. R., AND V. F. ESTOP. 1976. Notes on the estimation of alate aphid populations using Moericke yellow trays. Phil. Entomol. 3: 246-249.
  • GERAUD, F. 1976. El áfido negro de los cítricos Toxoptera citricida (Kirkaldy) en Venezuela (Resumen). Premier Encuentro Venezuelano de Entomologia. Universidad central de Venezuela. Faculdad de Agronomia-Instituto de Zoologia Agricola. Maracay, Venezuela.
  • KAUFMAN, O. 1932. Einige Bemerkungen uber den Einfluss von Temperaturschwankungen auf die Entwicklungsdauer und Streuung bei Insekten und eine graphische Darstellung durch kettelinie und Hyperbel. Z. Morphol Oekol. Tiere 25: 352-361.
  • HALBERT, S. E., AND L. G. BROWN. 1996. Toxoptera citricida (Kirkaldy), brown citrus aphid - identification, biology and management strategies. Cir. No. 374. Div. Plant Industry, Entomol. Fla. Dept. Agric. and Cons. Serv.
  • HALIMA, K. M. B., J. M. RABASSE, AND M. H. B. HAMOUDA. 1994. The aphids of citrus fruits and their natural enemies in Tunisia. Tropicultura 12: 145-147 (in Port., Eng. sum).
  • HALL, W. J. 1930. Notes on the control of some of the more important insect pests of citrus in Rhodesia. Rhodesia Agric. J. 27: 737-747.
  • HELY, P. C. 1968. The entomology of citrus in New South Wales. Misc. Pub. Aust. Entomol. Soc. 1: 1-20.
  • KHAN, M. H. 1976. The citrus aphid, Toxoptera citricidus (Kirk.). Bien. Rep. Waite Agr. Res. Inst. 1976-77, p. 100. Univ. of Adelaide, South Australia.
  • KIRKALDY, G. W. 1907. On some peregrine Aphidae in Oahu, Honolulu. Proc. Hawaiian Entmolog. Soc. 1:100.
  • KLAS, F. E. 1979. Population desnities and spatial patterns of the aphid tristeza vector, Toxoptera citricida Kirk. Proc. Eighth I.O.C.V. Conf. Pp. 83-87.
  • KNORR, L. C., AND S. MOIN SHAH. 1971. World citrus problems V. Nepal. F.A.O. Pl. Prot. Bull. 19: 73-79.
  • KOLI, S. Z., K. G. CHOUDHARI, AND P. V. MAKAR. 1978. Comparative study on residual toxicity of some insecticides against citrus aphid, Toxoptera citricidus Kirk. J. Mahar. Agric. Univ. 3: 273.
  • KOMAZAKI, S. 1982. Effects of constant temperatures on population growth of three aphid species, Toxoptera citricidus (Kirkaldy), Aphis citricola van der Goot and Aphis gossypii Glover (Homoptera: Aphididae) on citrus. Appl. Entomol. Zool. 17: 75-81.
  • KOMAZAKI, S. 1988. Growth and reproduction in the first two summer generations of two citrus aphids, Aphis citricola van der Goot and Toxoptera citricidus (Kirkaldy) (Homoptera: Aphididae), under different thermal conditions. Appl. Entomol. Zool. 23: 220-227.
  • KOMAZAKI, S., Y. SAKAGAMI, AND R. KORENGA. 1979. Overwintering of aphids on citrus trees. Jpn. J. Entomol. Zool. 23: 246-250. (in Jap., Eng. sum.).
  • LAING, F. 1927. Coccidae, Aphididae and Aleyrodidae. P. 34-45 in Insects of Samoa II. Brit. Mus. Nat. His., London.
  • LASTRA, R., R. LEE, M. A. ROCHA-PENA, C. L. NIBLETT, S. M. GARNSEY, AND R. K. YOKOMI. 1992. Survey for presence of tristeza virus and Toxoptera citricidus in Mexico and Central America. CATIE-University of Florida-INIFAP/SARH-USDA, Turrialba, Costa Rica.
  • LASTRA, R., R. MENESES, P. E. STILL, AND C. L. NIBLETT. 1991. The citrus tristeza virus situation in Central America. p. 156-159 in R. H. Brlanski, R. F. Lee, and L. W. Timmer [eds.], Proc. Conf. Intl. Org. Citrus Virol. 11th, Riverside, California.
  • LEE, R. F., R. H. BRLANSKY, S. M. GARNSEY, AND R. K. YOKOMI. 1987. Traits of citrus tristeza virus important for mild strain cross protection of citrus: the Florida approach. Phytophylactica 19:215-218.
  • LEE, R. F., K. S. DERRICK, C. L. NIBLETT, AND H. R. PAPPU. 1995. When to use mild strain cross protection (MSCP) and problems encountered. P. 158-161 In: Proceedings of the Third International Workshop. Citrus Tristeza Virus and the Brown Citrus Aphid in the Caribbean Basin: Management Strategies, May 15-18, Lake Alfred, FL. CREC, Lake Alfred, FL 269 pp.
  • LEE, R. F., P. LEHMANN, AND L. NAVARRO. 1998. Nursery practices, budwood and rootstock certification programs. In: Citrus Health Guide. L. W. Timmer and L. Duncan, Eds. APS Press, Minn. In press.
  • LEE, R. F. AND M. A. ROCHA-PENA. 1992. Citrus tristeza virus. In: Plant Diseases of International Importance. Vol. III. A. N. Mukhopadhyay, H. S. Chaube, J. Kumar, and U. S. Singh, Eds. Pp 226-249. Prentice Hall, New Jersery
  • LEVER, R. J. A. W. 1940. Insect pests of citrus, pineapple and tobacco. Agric. J. Fiji 11: 99-101.
  • MAMET, R. 1939. The Aphididae of Mauritius. Mauritius Inst. Bull. 1: 43-56.
  • Marais, L. J. 1994. Citrus tristeza and its effect on the Southern Africa. Citrus Industry 75(6): 58-60
  • MICHAND, J. P. 1998. A review of the literature on Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Fla. Entomol. 81: 37-61.
  • MOREIRA, S. 1967. Outbreaks and new records F.A.O.Pl. Prot. Bull. 15: 59-60.
  • NAKAO, S. 1968. Ecological studies on the insect community of citrus groves IV. A list of insects collected in a citrus grove near Fukuoka City. Kontyû: 30: 50-71.
  • NICKEL, O., AND F. KLINGAUF. 1985. Biologie und massenwechsel der tropischen citrus-blattlaus Toxoptera citricidus in beziehung zu Nützlingsaktivität und klima in Misiones Argentinien (Homoptera: Aphididae). Entomol. Gener. 10: 231-240. (in Germ., Eng. sum.).
  • POPRAWSKI, T. J., P. E. PARKER, AN J. H. TSAI. 1999. Laboratory and field evaluation of hyphomycete insect pathogenic fungi for control of brown citrus aphid (Homoptera: Aphididae) Environ. Entomol. 28: (In press).
  • PORTILLO, M. M. 1977. Acción del aficida pirimicarb en el pulgon de los citrus Toxoptera citricidus (Kirkaldy) y en el coccinélido predador Cyloneda sanguinea (L.). Idia 331/333: 63-66.
  • ROISTACHER, C. N. 1981. A blueprint for disaster. Part 2: Changes in transmissibility of seedling yellows. Calif. Citrogr. 67: 28-32.
  • ROCHA-PENA, M. A., R. F. LEE, R. LASTRA, C. L. NIBLETT, F. M. OCHOA-CORONA, S. M. GARNSEY, AND R. K. YOKOMI. 1995. Citrus tristeza virus and its aphid vector Toxoptera citricida: Threats to citrus production in the Caribbean and Central and North America. Plant. Dis. 79: 437-443.
  • ROISTACHER, C. N. 1988. Observations on the decline of sweet orange trees in coastal Peru caused by stem-pitting tristeza. Pl. Prot. Bull., India 36: 19-26.
  • ROISTACHER, C. N., AND M. BAR-JOSEPH. 1987. Aphid transmission of citrus tristeza virus: A review. Phytophylactica 19: 163-167.
  • SCHOULTIES, C. L., L. G. BROWN, C. O. YOUTSEY, AND H. A. DENMARK. 1987. Citrus tristeza virus and vectors: Regulatory concerns. Proc. Fla. State. Hort. Soc. 100: 74-76.
  • SCHWARZ, R. E. 1965. Aphid-borne virus diseases of citrus and their vectors in South Africa. B. Flight activity of citrus aphids. S. Afr. Agric. Sci. 8: 931-940.
  • SEIF, A. A., AND A. S. ISLAM. 1988. Population densities and spatial distribution patterns of Toxoptera citricida (Kirk.) (Aphididae) in Citrus at Kenya coast. Insect. Sci. Appl. 9: 535-538.
  • SQUIRE, F. 1972. Entomological problems in Bolivia. P.A.N.S. 18: 249-268. British Mission in Tropical Agriculture, Cochabamba, Bolivia.
  • STOETZEL, M. B. 1994. Aphids (Homoptera: Aphididae) of potential importance on citrus in the United States with illustrated keys to species. Proc. Entomol Soc. Wash. 96: 74-90.
  • SYMES, C. B. 1924. Notes on the black citrus aphis. Rhodesia Agric. J. 11: 612-626.
  • TAKAHASHI, R. 1926. Some Aphididae of Sumatra. 2. Treubia 8: 426-466.
  • TAKANASHI, M. 1989. The reproductive ability of apterous and alate viviparous morphs of the citrus brown aphid, Toxoptera citricidus (Kirkaldy) (Homoptera: Aphididae). Jap. J. Appl. Entomol. Zool. 33: 266-269. (in Jap., Eng. sum.).
  • TAO, C. C., AND C. CHIU. 1971. Biological control of citrus, vegetable and tobacco aphids. Spec. Publ. Taiwan Agric. Res. Inst. 10: 1-110.
  • TAO, C. C. AND M. F. TAN. 1961. Identification, seasonal population and chemical control of citrus aphids in Taiwan. Agric. Res. 10: 41-52.
  • TAO, C. C., AND K. C. WU. 1968. Report on citrus insect control study by chemicals in Taiwan. Pl. Prot. Bull, Taiwan 10: 57-64. (in Chin., Eng. sum.).
  • TAO, C. C., AND K. C. WU. 1969. Studies on bark treatment against citrus insects. Pl Port. Bull. Taiwan 11: 143-149. (in Chin., Eng. sum.).
  • THEOBALD, F. V. 1928. Aphididae from Italian Somaliland and Eritrea. Bull. Entomol. Res. 11: 177-180.
  • TSAI, J. H. 1998. Development, survivorship, and reproduction of Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae) on eight host plants. Environ. Entomol. 27: 1190-1195.
  • TSAI, J. H., AND K. H. WANG. 1999. Life table study of brown citrus aphid, Toxoptera citricida (Homoptera: Aphididae) at eight constant temperatures. Environ. Entomol. 28 (In press).
  • VAN DER GOOT, P. 1918. Aphididae of Ceylon . Spolia Zeylanica, Columbo 11: 70-75.
  • VAN HOOF, H. A. 1961. Observations on aphid flights in Suriname. Entomol. Exp. Appl. 5: 239-243.
  • YOKOMI, R. K., AND S. M. GARNSEY. 1987. Transmission of citrus tristeza virus by Aphis gossypii and Aphis citricola in Florida. Phytophylactica 19: 169-172.
  • YOKOMI, R. K., S. M. GARNSEY, R. F. LEE, AND M. COHEN. 1987. Use of insect vectors to screen for protecting effects of mild citrus tristeza virus isolates in Florida. Phytophylactica 19:183-185.
  • YOKOMI, R. K., R. LASTRA, M. B. STOETZEL, R. F. LEE, S. M. GARNSEY, T. R. GOTTWALD, M. A. ROCHA-PENA, AND C. L. NIBLETT. 1994. Establishment of the brown citrus aphid (Homoptera: Aphididae) in Central America and the Caribbean basin and transmission of citrus tristeza virus. J. Econ. Entomol. 87: 1078-1085.
  • YOKOMI, R. K., P. A. STANSLY, E. A. RODRIGUEZ, AND T. R. GOTTWALD. 1995. Chemical mitigation of brown citrus aphid populations in Puerto Rico. p 75-76 in Proceedings of the Third International Workshop on Citrus Tristeza Virus and Brown Citrus Aphid in the Caribbean Basin: Management Strategies. Lake Alfred, FL, May 15-18, 1995. University of Florida, Institute of Food and Agricultural Sciences.