EPPO Datasheet: Aphis citricidus
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Aphididae
Other scientific names: Aphis aeglis Shinji, Aphis nigricans van der Goot, Aphis tavaresi Del Guercio, Myzus citricidus Kirkaldy, Paratoxoptera argentiniensis Blanchard, Toxoptera aphoides van der Goot, Toxoptera citricida (Kirkaldy), Toxoptera citricidus (Kirkaldy), Toxoptera tavaresi (Del Guercio)
Common names in English: brown citrus aphid, oriental black citrus aphid, tropical citrus aphid
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Notes on taxonomy and nomenclature
Aphis citricidus was described as Myzus citricidus because of its resemblance to Myzus cerasi according to its author (Kirkaldy, 1907). A few years later it was transferred to the genus Aphis and later to the genus Toxoptera. It has now been returned to the genus Aphis, because Toxoptera was synonymized with Aphis by Lagos et al. (2014), as a result of the study of 41 morphological characteristics and the sequences of COI and EF1-α of 68 species of the subtribe Aphidina. Nieto Nafría et al. (2011) established that citricidus is the correct specific epithet for the species, instead of citricida, which was frequently used. For much of the 20th century, A. citricidus has often been confused with A. aurantii Boyer de Fonscolombe, the black citrus aphid, several records of the latter applying to A. citricidus.
EU Categorization: A2 Quarantine pest (Annex II B)
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EPPO Code: TOXOCI
Aphis citricidus preferentially feeds on Citrus species (Rutaceae) and also on other Rutaceae; Blackman & Eastop (2021) specifically list C. aurantiifolia, C. aurantium, C. glauca, C. limon, C. maxima, C. media, C. reticulata and C. sinensis.
A. citricidus is catalogued as a polyphagous aphid, with a preference for the Rutaceae, although it may be limited to colonizing young growth of plants of other families, on which it can establish dense colonies. Blackman & Eastop (2021). In Northern Spain, Hermoso de Mendoza et al. (2008) occasionally found high populations levels of the aphid on Chaenomeles speciosa (Rosaceae) which is cultivated as an ornamental. Michaud (1998) listed 28 plant families (including Rutaceae) on which A. citricidus has been observed.Host list: Artabotrys hexapetalus, Artocarpus altilis, Atalantia buxifolia, Berberis sp., Boehmeria sp., Bombax ceiba, Bougainvillea spectabilis, Bridelia ovata, Calodendrum capense, Camellia japonica, Cassia sp., Chaenomeles lagenaria, Chamaecrista absus, Choisya ternata, Cinnamomum camphora, Citrus aurantiifolia, Citrus aurantium, Citrus glauca, Citrus jambhiri, Citrus karna, Citrus limon, Citrus maxima, Citrus medica, Citrus paradisi, Citrus reticulata, Citrus sinensis, Clausena lansium, Cleistanthus monoicus, Clutia abyssinica, Coffea arabica, Commiphora mollis, Cotoneaster sp., Crataegus sp., Dianthus sp., Dioscorea rotundata, Diospyros kaki, Engelhardia spicata, Eriobotrya sp., Eurya japonica, Ficus carica, Ficus ingens, Ficus retusa, Flindersia xanthoxyla, Fortunella margarita, Geijera parviflora, Gonostegia hirta, Gossypium hirsutum, Ipomoea staphylina, Lasianthus chinensis, Limonia acidissima, Litsea monopetala, Loranthus sp., Maclura cochinchinensis, Maclura tricuspidata, Maesa chisia, Magnolia sp., Malpighia glabra, Malus domestica, Malus sylvestris, Mangifera indica, Murraya paniculata, Nicotiana tabacum, Oxalis pes-caprae, Passiflora foetida, Poncirus trifoliata, Pyrus communis, Quercus griffithii, Rhododendron sp., Rhus sp., Rorippa indica, Rubia cordifolia, Samanea saman, Schima wallichii, Solanum aligerum, Terminalia catappa, Tetradium daniellii, Toxicodendron khasianum, Trema orientale, Triphasia trifolia, Ulmus procera, Vepris lanceolata, Viburnum foetidum, Xylosma congesta, Zanthoxylum armatum, Zanthoxylum asiaticum, Zanthoxylum fagara, x Citrofortunella floridana, x Citrofortunella microcarpa
GEOGRAPHICAL DISTRIBUTION 2021-06-07
A. citricidus is thought to originate from South-East Asia (Michaud, 1998) and occurs predominantly in humid tropical regions. Hermoso de Mendoza et al. (2008) presented the history of the dispersal of the species from Asia to many other parts of the world with citrus plants. It is widespread in Africa south of the Sahara, and also present in Australia, New Zealand, and the Pacific Islands. It has also spread to citrus-growing areas in Central America, the Caribbean and Southern USA (Halbert, 1996). In the early 2000s, it was first found in Mediterranean Basin, in Northern Portugal and Northern Spain.
A. citricidus thrives in moist warm climates and seems able to tolerate colder conditions than A. aurantii, for example occurring at higher altitudes, but it is not found in regions with long hot dry seasons (Blackman & Eastop, 2021). It is known to occur in territories with a Mediterranean climate (in Europe, North America, South America, Africa and Australia) and even in territories with a Euro-Atlantic climate with mild winters, such as Northern Portugal, Galicia and the northern slopes of the Cantabrian Mountains in Spain (Ilharco et al., 2005; Hermoso de Mendoza et al., 2008).EPPO Region: Portugal (mainland, Madeira), Spain (mainland)
Africa: Angola, Benin, Burundi, Cameroon, Central African Republic, Congo, Congo, Democratic republic of the, Cote d'Ivoire, Eswatini, Ethiopia, Ghana, Guinea, Kenya, Malawi, Mauritius, Mozambique, Nigeria, Reunion, Rwanda, Saint Helena, Senegal, Seychelles, Sierra Leone, Somalia, South Africa, Sudan, Tanzania, Togo, Uganda, Zambia, Zimbabwe
Asia: Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China (Chongqing, Fujian, Guangdong, Guangxi, Guizhou, Hainan, Jiangsu, Shaanxi, Shandong, Sichuan, Xianggang (Hong Kong), Yunnan, Zhejiang), India (Arunachal Pradesh, Assam, Delhi, Karnataka, Maharashtra, Manipur, Meghalaya, Odisha, Punjab, Sikkim, Tamil Nadu, Uttar Pradesh, West Bengal), Indonesia (Irian Jaya, Java, Sulawesi, Sumatra), Japan (Honshu, Kyushu, Ryukyu Archipelago, Shikoku), Korea Dem. People's Republic, Korea, Republic, Laos, Malaysia (Sabah, Sarawak, West), Myanmar, Nepal, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam
North America: Mexico, United States of America (Florida, Hawaii)
Central America and Caribbean: Antigua and Barbuda, Aruba, Belize, Bermuda, Cayman Islands, Costa Rica, Cuba, Dominica, Dominican Republic, Grenada, Guadeloupe, Guatemala, Haiti, Honduras, Jamaica, Martinique, Netherlands Antilles, Nicaragua, Panama, Puerto Rico, Saint Lucia, St Kitts-Nevis, St Vincent and the Grenadines, Trinidad and Tobago, Virgin Islands (British), Virgin Islands (US)
South America: Argentina, Bolivia, Brazil (Amapa, Bahia, Ceara, Espirito Santo, Goias, Maranhao, Mato Grosso do Sul, Minas Gerais, Para, Parana, Pernambuco, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, Sao Paulo), Colombia, Ecuador (Galapagos), French Guiana, Guyana, Paraguay, Peru, Suriname, Uruguay, Venezuela
Oceania: Australia (New South Wales, Queensland, South Australia, Tasmania, Victoria, Western Australia), Cook Islands, Fiji, French Polynesia, New Zealand, Papua New Guinea, Samoa, Solomon Islands, Tonga, Vanuatu
Aphis citricidus is an anholocyclic aphid (i.e. its annual life cycle is completed without sexual generation) everywhere except in Japan (Komazaki, 1988). Generations of parthenogenetic and viviparous females follow one another continuously and, as in almost all aphids, the birth of the first daughter of a female occurs shortly after the end of the imaginal molt, and successive births occur very rapidly.
Galatoire (1983), Takahashi (1989), Michaud, (1998) and Shang et al. (2016) among others, report details on life cycle, population dynamics and flight dispersal. In Northern Spain, Hermoso de Mendoza et al. (2008) report that the populations of the species were maintained parthenogenetically with production of alate viviparous females throughout the study period (June 2002 to October 2007). They concluded from the trapped alata that each year there was a long minimum period of flight in winter and another short minimum period in midsummer, and one or two maxima in the passage from spring to summer and another maximum in autumn.
A citricidus is considered to be the most efficient vector of citrus tristeza virus (CTV), a phloem-limited closterovirus. In particular, it can transmit the most aggressive strains of CTV causing quick decline and stem-pitting (Hermoso de Mendoza et al. (2008). CTV is transmitted by A. citricidus is a semi-persistent mode.
DETECTION AND IDENTIFICATION 2021-06-07
Growth of citrus shoots is greatly impaired, and they become distorted; leaves become brittle and wrinkled and curl downwards. Attacked flowers fail to open or do so abortively since the ovaries are deformed.
Apterae are 1.5–2.4 mm long, very dark shiny brown to shiny black and with antennas partially dark (proximal and distal segments) and light (intermediate segments). According to Blackman & Eastop (2021), the best characters to differentiate the apterous viviparous females of A. citricidus from those of A. aurantii are: longest seta on antennal segment III 29–64 µm in A. citricidus versus 12–27 in A. aurantii; longest seta on hind tibia 80 µm at least in A. citricidus versus 60 µm at most in A. aurantii.
Alatae have a shiny black abdomen, with a wholly black third antennal segment succeeded by a pale fourth segment (which carry respectively 6 to 20 and sometimes 1 to 4 secondary sensoria), front wing pterostigma is brown but paler than the distal part of femora and median vein of front wing is twice-branched. In A. aurantii the pterostigma is as dark brown to black as the femora, and the median vein is one-branched.
Both morphs have long (about 1/6 body length), truncated-conical and strongly sculptured siphunculi, and thick and bluntly rounded at the apex cauda, with very long setae.
A useful character to distinguish A. citricidus from A. aurantii is that disturbed colonies of the latter produce a distinct scraping sound, audible from up to 45 cm from the leaf, whereas those of A. citricidus do not. In addition, specimens of A. citricidus in a small volume of alcohol turns the liquid deep red gradually, whereas specimens of other species of subgenus Toxoptera do not.
Detection and inspection methods
In countries where A. citricidus occurs or may occur, citrus groves should be meticulously inspected when leaf and flower buds emerge and grow.
The use of yellow water traps (a yellow basin filled at 2/3 of its capacity with water and a few drops of a surfactant product) are very useful to detect alate viviparous females at the beginning of the vegetative development season of the crops. Many aphids can fall in them, but the identification of alata of A. citricidus is not particularly complicated.
Plants that are transported must be carefully checked whatever their stage of development. Foliage should also be examined for dead, parasitized aphids or mummies, which adhere to the leaves and can be used for identification in the absence of living specimens.
If the aphid cannot be positively identified on the spot using a pocket lens, specimens should be preserved in ethanol. It is adequate to use 70% ethanol to transport the specimens to the laboratory and observe them with the stereomicroscope, to make microscopic preparations, to store them or send them to a specialist. For mitochondrial COII analysis, specimens must be preserved in 96-99% ethanol.
Guidance on the morphological identification of A. citricidus can be found in the EPPO diagnostic protocol (EPPO, 2006).
PATHWAYS FOR MOVEMENT 2021-06-07
A. citricidus can spread locally by flight. Over long distances, the main pathway for introducing A. citricidus into new areas is the movement of plants for planting (EFSA, 2018). It has been intercepted, but very infrequently, in mainland USA on citrus from Hawaii and the Philippines. It is more strongly attracted to yellow than many other aphids and it may therefore be transported on yellow packaging or aircraft parts.
PEST SIGNIFICANCE 2021-06-07
Aphis citricidus per se causes considerable damage to citrus trees by attacking shoots and flowers and sometimes young fruit. Even a few aphids on a young shoot will arrest blossom bud development and cause them to fall. Losses of up to 50% can result from feeding damage (Kranz et al., 1977). After petal fall, however, growing plant parts harden and this results in less damage, even at relatively high population levels. As is the case for other Aphis species, sooty mold forms on the aphid honeydew, interfering with leaf photosynthesis and forming unsightly deposits on fruits, which reduces their market value.
Citrus tristeza virus (CTV) is transmitted by several species of aphids (e.g. Aphis gossypii, A. spiraecola, A. aurantii, A. craccivora and Myzus persicae) through a semi-persistent transmission mode, but certainly A. citricidus is the most efficient CTV vector. Therefore, most of the losses produced by this virus infection in the countries where A. citricidus is found are indirectly attributable to it. This aphid also transmits citrus vein-enation disease in South Africa.
Control measures are intended to prevent damage to young shoots and fruits, and especially to suppress the formation of alatae, which are liable to transmit viruses (Kranz et al., 1977). Applications of authorized insecticides on affected plants are recommended for treatment of recognized foci. Young trees can be treated preventively with systemic insecticides. Many natural enemies are known, some parasitoids (e.g. Lysiphlebus testaceipes and Lipolexis oregmae, both Hymenoptera: Braconidae) are being used in integrated control programs (Zamora Mejias, 2011). In Northern Spain, Hermoso de Mendoza et al. (2008) cited a plethora of natural enemies that acted on populations of A. citricidus: 5 species of Aphidiinae (Hymenoptera: Braconidae), 1 of Cecidomyidae, 1 of Chamaemyiidae and 6 of Syrphidae (Diptera), 2 of Chrysopidae (Neuroptera), 5 of Coccinellidae (Coleoptera), 1 of Anthocoridae (Hemiptera) and 1 of Trombidiidae (Acari: Trombidiformes).
Since A. citricidus has become established in several areas of the world with a Mediterranean climate, it probably has the potential to survive in most Mediterranean countries. The polyphagy of the species increases the risk that an aphid species can invade a territory, establish and spread there. The main risk for Mediterranean countries is the fact that it is a more efficient vector of citrus tristeza virus than the native aphid species or other introduced species, such as Aphis gossypii. A. citricidus is already present in the Iberian Peninsula, but far from the extensive citrus cultivation areas. Its introduction into new areas would cause serious problems to citrus production, as well as for citrus certification schemes, by creating a much higher risk of reinfection of certified material by tristeza.
PHYTOSANITARY MEASURES 2021-06-07
Importation of Citrus plants for planting is prohibited or restricted in many EPPO countries to prevent introduction of important pests. If not prohibited, it can be recommended that plants for planting of citrus and other potential hosts should come from a pest-free area or a pest-free place of production. For citrus fruit, it is generally required that they should be free from peduncles and leaves and this should cover the risk of transporting the pest into new areas, as A. citricidus does not feed on mature fruit.
Blackman RL & Eastop VF (2021) Aphids on the World’s plants. An online identification and information guide. http://www.aphidsonworldsplants.info/
CABI (1998) Distribution Maps of Pests No. 132. Toxoptera citricidus (Kirkaldy). CABI, Wallingford, UK.
EPPO (2006) EPPO Standard. Diagnostics. PM 7/75(1) Toxoptera citricidus. EPPO Bulletin 36, 451-456.
EFSA (2018) EFSA Plant Health Panel. Scientific opinion on the pest categorisation of Toxoptera citricida. EFSA Journal 16(1), 5103, 22 pp. https://doi.org/10.2903/j.efsa.2018.5103
Galatoire I (1983) Vital statistics of Toxoptera citicidus (Kirkaldy) (Homoptera Aphididae). Revista de la Sociedad Entomológica Argentina 42, 353-368.
Hermoso de Mendoza A, Álvarez A, Michelena JM, González P, Cambra M (2008) Dispersión, biología y enemigos naturales de Toxoptera citricida (Kirkaldy) (Hemiptera, Aphididae) en España. Boletín de Sanidad Vegetal Plagas 34, 77-87.
lharco FA, Sousa-Silva CR, Álvarez Álvarez A (2005) First report on Toxoptera citricidus (Kirkaldy) in Spain and continental Portugal (Homoptera, Aphidoidea). Agronomia Lusitana 51, 19-21.
Komazaki S (1988) [Citrus aphid population studies]. Applied Entomology and Zoology 23, 220-227.
Lagos DM, Voegtlin DJ, Coeur d’acier A, Giordano R (2014) Aphis (Hemiptera: Aphididae) species groups found in the Midwestern United States and their contribution to the phylogenetic knowledge of the genus. Insect Science 21, 374–391. https://doi.org/10.1111/1744-7917.12089
Michaud JP (1998) A review of the literature on Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Florida Entomologist 81(1), 37-61.
Nieto Nafría JM, Alonso-Zarazaga MA, Pérez Hidalgo N (2011) Toxoptera citricida or Toxoptera citricidus? The validity of a specific name (Hemiptera, Aphididae, Aphidini). Graellsia 61, 141-142.
Shang F, Ding B-Y, Xiong Y, Dou W, Wei D, Jiang H-B., Wei D-D, Wang J-J (2016) Differential expression of genes in the alate and apterous morphs of the brown citrus aphis, Toxoptera citricida. Scientific Reports 6, 32099. https://doi.org/10.1038/srep32099
Takahashi (1989) The reproductive ability of apterous and alate viviparous morphs of the citrus brown aphid, Toxoptera citricidus (Kirkaldy (Homoptera: Aphididae). Japanese Journal of Applied Entomology and Zoology 34, 237-243.
Zamora Mejias D, Hanson PE, Starý P (2011) Parasitoid (Hym., Braconidae, Aphidiinae) complex of the black citrus aphid, Toxoptera citricidus (Kirkaldy) (Hem., Aphididae) in Costa Rica and its relationships to nearby areas. Journal of Entomological Research Society 13, 107-115.
This datasheet was extensively revised in 2021 by J. M. Nieto Nafría (honorary emeritus professor of Zoology. Universidad de León, Leon (Spain). His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2021-06-07
This datasheet was first published in the EPPO Bulletin in 1980 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.
CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).
EPPO (1980) Data sheets on quarantine organisms No. 45, Toxoptera citricidus. EPPO Bulletin 10(1), 4 pp. https://doi.org/10.1111/j.1365-2338.1980.tb02699.x