Toxoptera citricida (black citrus aphid)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Species Vectored
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Toxoptera citricida (Kirkaldy)
Preferred Common Name
- black citrus aphid
Other Scientific Names
- Aphis aeglis Shinji
- Aphis citricidus (Kirkaldy)
- Aphis nigricans van der Goot
- Aphis tavaresi Del. Guercio
- Myzus citricidus Kirkaldy
- Paratoxoptera argentiniensis EE Blanchard
- Toxoptera aphoides van der Goot
- Toxoptera citricidus Kirkaldy
- Toxoptera tavaresi (Del Guercio)
International Common Names
- English: brown citrus aphid; citrus aphid; tropical citrus aphid
- Spanish: afido moreno de los cítricos; afido vector de la tristaza en citricos; piojo de los citricos; pulgón citricida (Mexico); pulgón de la tristeza; pulgón marrón; pulgón negro de los cítricos; pulgón negro de los citros
- French: puceron noir de l'oranger; puceron toxoptere citricide
- Chinese: he juya
Local Common Names
- Brazil: pulgao preto da laranjeira
- Germany: Braune Zitrus-Blattlaus; Braune Zitruslaus
- Japan: abura mushi; mikan-kuro-aburamusi
- APHICI (Aphis citricidus)
- TOXOCI (Toxoptera citricida)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Uniramia
- Class: Insecta
- Order: Hemiptera
- Suborder: Sternorrhyncha
- Unknown: Aphidoidea
- Family: Aphididae
- Genus: Toxoptera
- Species: Toxoptera citricida
Notes on Taxonomy and NomenclatureTop of page
DescriptionTop of page
Winged adult female (alata): 1.1-2.6 mm in length; antennae six segmented with I, II, and III heavy black and other segments banded at joints, secondary rhinaria 7-20 on III and 0-4 on IV, setae on antennae III subequal to or exceeding diameter of segment; siphunculi black, elongate; cauda black, elongate with 25-40 setae; stridulatory apparatus on abdomen present; forewing with pterostigma light brown and media usually twice-branched.
Wingless adult female (aptera): 1.5-2.8 mm in length; oval; antennae six segmented with no secondary rhinaria; segments not banded, but segments I and II black, segments III and IV pale and slightly swollen, and segments V and VI dark at least at joints, setae on antennae III at least as long as the diameter of the segment; siphunculi black, elongate, and only slightly longer than cauda; cauda black and elongate with about 30 setae; 'knees' of all three pairs of legs very dark; stridulatory apparatus present.
DistributionTop of page
Although the aphid is tropical/subtropical in origin, the presence of a sexual stage and overwintering as eggs in Japan (Komazaki, 1982) suggests that T. citricida can adapt to different climates. Due to the restricted host range of the aphid to citrus and its relatives, the most favourable citrus environs for T. citricida occur when weather is warm and humid resulting in frequent stimulation of new growth cycles. Similarly, desert/semi-arid and cooler regions provide conditions favourable for T. citricida only seasonally. Populations typically increase rapidly following colony initiation resulting in crowding, a decline in host suitability, and production of winged (alate) aphids. Winged morph production could also be triggered by the physiology of the host. However, a key requirement for spread of T. citricida is that the alata must alight on citrus with new shoot growth to successfully establish a new colony.
A record for Iran in CABI/EPPO (1998) is an error; the species reported in the literature was T. aurantii and not T. citricida.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 30 Jun 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Central African Republic||Present|
|Congo, Democratic Republic of the||Present|
|Congo, Republic of the||Present|
|South Africa||Present, Widespread|
|Iran||Absent, Invalid presence record(s)|
|Cyprus||Absent, Invalid presence record(s)|
|Italy||Absent, Invalid presence record(s)|
|Malta||Absent, Invalid presence record(s)|
|Netherlands||Absent, Confirmed absent by survey|
|Antigua and Barbuda||Present, Few occurrences||1993|
|British Virgin Islands||Present|
|Costa Rica||Present, Localized|
|Netherlands Antilles||Present, Localized|
|Puerto Rico||Present, Localized||1992|
|Saint Kitts and Nevis||Present, Localized||1993|
|Saint Vincent and the Grenadines||Present, Widespread||1993|
|Trinidad and Tobago||Present, Widespread||First reported: 198*|
|U.S. Virgin Islands||Present, Localized|
|United States||Present, Localized|
|-New South Wales||Present|
|New Zealand||Present, Localized|
|Papua New Guinea||Present|
|-Mato Grosso do Sul||Present|
|-Rio de Janeiro||Present|
|-Rio Grande do Sul||Present|
|Chile||Absent, Invalid presence record(s)|
Hosts/Species AffectedTop of page
The aphid may be able to survive on some non-rutaceous hosts temporarily as they migrate away from a crowded food source (Yokomi et al., 1994). Athough Rutaceae are the preferred hosts, large colonies of apterae are often found on very different plants including Pyracantha (Rosaceae) in Malawi and Zimbabwe; Cudramia (Moraceae) in China and Australia; tea in the Seychelles; and Maclura (Moraceae) in Java.
Host Plants and Other Plants AffectedTop of page
|Citrus aurantiifolia (lime)||Rutaceae||Main|
|Citrus limon (lemon)||Rutaceae||Main|
|Citrus maxima (pummelo)||Rutaceae||Main|
|Citrus medica (citron)||Rutaceae||Unknown|
|Citrus nobilis (tangor)||Rutaceae||Main|
|Citrus reticulata (mandarin)||Rutaceae||Main|
|Citrus reticulata x paradisi (tangelo)||Rutaceae||Main|
|Citrus sinensis (navel orange)||Rutaceae||Main|
|Citrus unshiu (satsuma)||Rutaceae||Main|
|Citrus x paradisi (grapefruit)||Rutaceae||Main|
Growth StagesTop of page
SymptomsTop of page
List of Symptoms/SignsTop of page
|Leaves / honeydew or sooty mould|
|Leaves / honeydew or sooty mould|
Species VectoredTop of page
Biology and EcologyTop of page
The major impact of T. citricida is due to its efficient transmission of Citrus tristeza virus (CTV) (Costa and Grant, 1951; Yokomi et al., 1994), a phloem-limited closterovirus (Bar-Joseph and Lee, 1989). Two types of CTV strains are economically important: those that cause decline of citrus budded onto sour orange (Citrus aurantium) rootstock; and those that cause stem pitting of grapefruit and sweet orange regardless of rootstock. Both are readily transmissible by T. citricida.
CTV is semipersistently transmitted by citrus aphids (Raccah et al., 1976). Aphids acquire virus from an infected trees with feeding times as short as 5-10 min; transmission efficiency increases with feeding times up to 24 h. There is no latent period and the virus does not multiply or circulate in the aphid. The time required to inoculate a plant is the same as for acquisition. The aphid is capable of spreading the virus for 24-48 hours without reacquisition (Meneghini, 1948). T. citricida also transmits Citrus vein enation (woody gall) virus, a probable luteovirus (da Graça and Maharaj, 1991), Cowpea aphid-borne mosaic virus, a potyvirus affecting groundnut in Brazil (Pio-Reheiro et al., 2000) and Celosia mosaic virus, a potyvirus affecting Celosea argentea in Nigeria (Owolabi et al., 1998). Migrating populations of T. citricida are also associated with the spread of certain nonpersistently-transmitted viruses such as Chilli veinal mottle virus (Blackman and Eastop, 1984) and Soybean mosaic virus in China (Halbert et al., 1986).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Aphelinus gossypii||Parasite||Adults; Arthropods|Nymphs|
|Coccinella octopunctata||Predator||Adults; Arthropods|Nymphs|
|Coccinella transversalis||Predator||Adults; Arthropods|Nymphs|
|Episyrphus balteatus||Predator||Adults; Arthropods|Nymphs||India||Citrus|
|Lecanicillium lecanii||Pathogen||Adults; Arthropods|Nymphs|
|Lipolexis gracilis||Parasite||Adults; Arthropods|Nymphs|
|Lipolexis scutellaris||Parasite||Adults; Arthropods|Nymphs|
|Lysiphlebia japonica||Parasite||Adults; Arthropods|Nymphs|
|Lysiphlebus mirzai||Parasite||Adults; Arthropods|Nymphs|
|Lysiphlebus testaceipes||Parasite||Adults; Arthropods|Nymphs|
|Mallada boninensis||Predator||Adults; Arthropods|Nymphs|
Notes on Natural EnemiesTop of page
The principal primary parasitoids of T. citricida are solitary endophagous Hymenoptera in the families Aphidiidae and Aphelinidae. The aphidiids are wasp-like in appearance and, at pupation, produce a mummy with a typical crusty golden, swollen appearance. They range in adult size from one to several millimetres. Adult Aphelinids are usually less than 1 mm, possess reduced wing venation and an abdomen which appears broadly attached to the thorax. They turn an aphid into a black mummy. Female adult aphelinids also feed on aphid haemolymph, a behaviour that is essential for completion of oogenesis. In Taiwan, T. citricida is parasitized by Lipolexis gracilis and L. scutellaris (Tao and Chiu, 1971), whereas in Australia it is parasitized by Aphelinus gossypii (Carver, 1978). In Japan, Lysiphlebia japonica is the principal parasitoid of T. citricida (Kato, 1970; Takanashi, 1990). In China, Lysiphlebia mirzai is a common parasitoid of T. citricida (Liu and Tsai, 2002).
Entomopathogenic fungi attack T. citricida and can decimate a population with dramatic speed. A critical requirement for efficacy of such fungi is high humidity. This is especially true when using Beauveria bassiana, Paecilomyces fumosoroseus and Metarhizium anisopliae against T. citricida (Poprawski et al., 1999). Verticillium lecanii has been reported to attack T. citricida in Venezuela (Rondón et al., 1980) and other fungi have been observed associated with the aphid in South Africa (Samways, 1984).
ImpactTop of page
T. citricida was the vector responsible for the rapid spread of CTV decline that caused death of many tens of millions of citrus trees (sour orange) in Brazil and Argentina in the 1930s and 1940s (Knorr and DuCharme, 1951) and in the 1970s in Colombia, Venezuela, and Peru over a 10-year period (Geraud, 1976; Lee et al., 1992). Currently in South Africa, T. citricida is spreading CTV strains that are so virulent that economic longevity of grapefruit has been shortened to 6-8 years even though it contains a cross-protecting CTV isolate (Marais et al., 1996). T. citricida was found to be 6 to 25 times more efficient in transmission of various CTV isolates than was Aphis gossypii (Yokomi et al., 1994). In Florida, USA, T. citricida is capable of separating severe strain (stem pitting strain) of CTV from the source plant affected with a mild strain of CTV following single aphid transmission (Tsai et al., 2000). Currently, there are an estimated 200 million citrus trees on sour orange rootstock worldwide and all are at immediate risk of CTV decline (Garnsey et al., 1996).
Detection and InspectionTop of page
Similarities to Other Species/ConditionsTop of page
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Management of virus inoculum is the most important control strategy (Garnsey et al., 1996) because spread of severe strains of Citrus tristeza virus (CTV) is the major problem associated with T. citricida. The first factor to consider is the prevalence of CTV and its strains in a particular area. If virulent stem pitting strains and T. citricida are endemic, citrus scion varieties tolerant to CTV should be planted. These include mandarins, pummelos, tangelos and tangor. Only CTV-tolerant or resistant rootstock should be used. Avoid planting grapefruit or Pera sweet orange unless they have been pre-infected with a cross-protecting CTV strain. If CTV strains are less virulent than the previous scenario, sweet oranges and grapefruit, preferably pre-inoculated with a mild CTV isolate, can be grown with consideration for the market targeted (e.g. fresh fruit, domestic, export, juice, etc.). When CTV problems are anticipated, closer plant spacing should be considered to maximize land use during the grove's early years. Trees that decline or become stunted can either be replaced or simply removed and neighbouring trees allowed to fill in.
Close plant spacing is becoming a common practice in new groves in the USA. Tree size is managed by mechanical hedgers that trim the sides and tops of trees. This practice produces conditions excellent for CTV spread and allows tree canopies to touch in the direction of the row. Pruning induces new shoot growth in which CTV multiplication is optimal as long as temperature and moisture are favourable. Citrus aphid migration, including that of T. citricida, peak in spring and autumn (Carver, 1978; Schwartz, 1965). Hence the uniform growth that results from pruning maximizes opportunities for CTV acquisition and inoculation.
If CTV incidence is undetectable or mild and T. citricida is not established in a particular region, citrus trees grafted on sour orange rootstock may still be acceptable (Garnsey et al., 1996). This decision depends on the risk of losses due to CTV versus the advantages gained by the use of sour orange (e.g. salinity, cold hardiness, Phytophthora, high soil pH, poor drainage). Several areas have managed CTV by eradication of infected trees (for example in Israel and California). This programme is cost effective if virus incidence is low and spread is slow (Garnsey et al., 1996).
Regardless of the present CTV/aphid vector situation, a citrus budwood certification programme is essential for a good citrus industry. CTV and all other citrus virus and virus-like agents are readily graft transmissible. Diagnostic methods are available for testing and detection of citrus pathogens in budwood sources. Recent developments in serology and molecular biology allow some rapid evaluation of pathogen virulence. Thermotherapy and shoot tip grafting are now standard methods to eliminate pathogens from budwood. If a cross-protective CTV isolates are available, they can be incorporated into the budwood certification programme.
Although natural enemies are important in regulating aphid populations, they alone may not be satisfactory for controlling plant virus diseases. Aphid populations on citrus are often too variable to provide sufficient natural enemies for effective vector control. One concept is to direct biological control activities to reduce migrant vector populations before they spread through susceptible crops (Mackauer, 1976). Given that alternative prey are available, natural enemies could reduce T. citricida populations to mitigate secondary spread of CTV (tree to tree within a field), especially if conservation and augmentation efforts are used. In Japan, Lysiphlebia japonica is the most important parasitoid of T. citricida (Takanashi, 1990). However, this parasite was imported and released in southern Florida with no success (Deng and Tsai, 1998). In China, Lysiphlebus mirzai is a common parasitoid of T. citricida (Liu and Tsai, 2002). In South America, various natural enemies have been observed attacking T. citricida but none has been used for augmentation in a biological control programme.
Lysiphlebus testaceipes was found attacking T. citricida in Puerto Rico, Cuba and southern Florida (Yokomi and Tang, 1996; Ravelo and Triana-Fernandez, 1997; Evans and Stange, 1997) but the rate of parasitism was low, as was previously observed in Australia (Carver, 1984). Murakami et al. (1984) did not find effective parasitoids of T. citricida in the Cerrados region of Brazil and suggested that L. japonica be imported and released against T. citricida. T. citricida was introduced in south Florida in the later half of 1995 and spread to all citrus-growing areas in just 3-4 years. Assuming that biological agents colonize new areas more slowly than their hosts, multiple augmentative releases of mass-reared parasitoids at various sites should be conducted (Wellings, 1994). A classical biological control effort undertaken using this strategy in Florida with the release of L. japonica and Aphelinus spiraecolae (Tang et al., 1996) has not been successful.
As most predators are generalist feeders, presence of alternative prey provides stability to their contribution as biological control agents. The spirea aphid Aphis spiraecola is a cosmopolitan species with a wide host range and is quick to colonize new citrus shoots (Cole, 1925; Miller, 1929; Tsai and Wang, 2001). This aphid also develops large populations rapidly on citrus which attracts predators. If T. citricida arrive when these predators are present, they readily attack T. citricida. However, if predators discover a T. citricida population shortly after colonization, their probability of establishment is low without alternative prey as another food source (Michaud, 1996). Several predators including lacewings (Chrysoperla plorabunda), syrphid fly (Pseudodorus clavatus) and coccinellid beetles (Coelophora inaequalis, Coccinella septempunctata, Cycloneda sanguinea, Harmonia axyridis, Hippodamia convergens, Olla v-nigrum and Coleomegilla maculata fuscilabris) have been evaluated in the field and laboratory with varying degrees of success (Michaud, 1999, 2000, 2001; Wang and Tsai, 2001).
There is limited information available on the host range of T. citricida and it is unknown if any citrus cultivars or citrus relatives are resistant to the aphid.
Insecticidal control of T. citricida to slow spread of CTV is an unproven strategy. Although insecticides may not act quickly enough to prevent primary infection by viruliferous aphids, reduction of aphid populations would decrease secondary spread. Its effectiveness depends on longevity of suppression and extent of the treated area in relation to inoculum reservoir and migratory activity of the aphid (Knapp et al., 1996). It should be cautioned that use of foliar insecticides can interfere with biological control agents and, ultimately, their use to protect citrus (a perennial crop) is temporary. In the continental USA, most CTV spread occurs during spring and autumn when temperatures are mild. This is concomitant with when CTV titre (virus replication) in infected citrus trees is highest and when shoot growth and migration of T. citricida peak. Therefore, this time frame should be targeted if chemical control is attempted. Several systemic insecticides including acephate imidacloprid and acetamiprid have been used against T. citricida with various residual effects (Yamamoto et al., 2000; Tsai, 1999). A recent study showed that neem seed extract (azadirachtin) had a marked effect on the survival, longevity and fecundity of T. citricida but not its parasitoid Lysiphlebus testaceipes (Tang et al., 2002).
CTV is transmitted only by vectors that colonize citrus because it is phloem-limited. Thus, its epidemiology resembles persistently transmitted viruses more in this regard than nonpersistently transmitted viruses. As vector control has been shown to limit spread of some luteoviruses (Gourmet et al., 1994) it could be expected to have some impact on CTV spread. However, no data exist to recommend chemical control for CTV control.
Integrated Pest Management
It is not clear what level of vector control is necessary to reduce spread of CTV. The typical integrated pest management (IPM) approaches do not apply for CTV control. Economic thresholds are contingent both on T. citricida population and CTV inoculum pressure. Host-plant resistance to the aphid is not available. A unique management strategy must be practised for CTV in the presence of T. citricida. A strong regulatory component is necessary, covering both propagation and inoculum control (detection and removal of wild and possibly urban reservoirs of CTV) (Garnsey et al., 1996; Halbert and Brown, 1996). Management (conservation and/or augmentation) of biological control agents is feasible. Insecticidal control of vector populations may be useful in specific situations such as in a citrus nursery, or to protect budwood sources. Some value may result from the use of selective insecticides working in tandem with natural enemies. In the final analysis, vector management should be one component of a disease management strategy including other available elements such as mild strain cross-protection; tolerant rootstocks; regulatory measures, isolation or protection of nursery stock; and citrus scions with tolerance or resistance to CTV (Garnsey et al., 1996). In areas where T. citricida and severe (stem pitting) strain of CTV are endemic, the practice of using mild CTV strain to cross protect the subseqent infection of stem pitting strain has been carried out on a commercial basis in South Africa, Australia, Brazil, Peru, Reunion Island, India and Japan (Rocha-Pena et al., 1995; Bederski and Aubert, 1999).
ReferencesTop of page
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