(Craw, 1890)
Taxonomic note
This species has been wrongly attributed to Coquillet over most of its history (Danzig, 1993). The description of A. citrina by Coquillett is inadequate and simply refers to 'the yellow scale' on orange (Nel, 1933). A. citrina is morphologically very similar to the Californian red scale, A. aurantii, and was considered to be a variety until Nel, 1933, raised it to specific level based on a comparative study of its ecology, biology and morphology.
Diagnosis
Scale cover of adult female 1.5-2.0 mm in diameter, circular, flat, semi-translucent, lemon yellow to yellow-brown, with the yellow body of the insect visible through the scale; exuviae central or subcentral and transparent AONCITL3.jpg . The margin of the scale is parchment-like. Adult female scale covers of A. aurantii are similar in appearance to those of A. citrina but differ in colour, being reddish-orange. Scale cover of male smaller than that of female, oval, with subcentral, transparent exuviae AONCITL.jpg .
AOCIL.jpg
Body of slide-mounted adult female with prosoma becoming highly sclerotized and expanded with maturity; eventually the lateral lobes may project further posteriorly than the apex of the pygidium AOCIO.jpg . (This reniform shape characterises the genera Aonidiella and Africonidia (Ben-Dov, 1990a), although Aspidiotus macfarlanei is also reniform (Williams and Watson, 1988). Abdominal segments without any prepygidial macroducts. Pygidium with paraphyses present, most or all no longer than median lobes; perivulvar pores absent; prevulvar apophyses present, prevulvar scleroses absent AOCITP.jpg ; and plates lateral to third lobes each fringed (not with a single fleshy process) AOCIMG.jpg .
Host range
Aonidiella citrina is polyphagous, attacking plant species belonging to more than 50 genera in 32 families (Borchsenius, 1966). The main hosts of economic importance are Citrus spp. but A. citrina is also recorded incidentally on a wide range of ornamentals and some fruit crops including tea (Camellia sinensis) and peach (Prunus persica). Host records include species of: Acacia, Ardisia, Aucuba, Camellia sinensis, Camellia, Citrus spp., Citrofortunella mitis, Citroncirus, Clematis hybrids, Cleyera, Cucurbitaceae, Cydonia, Daphne, Eucalyptus, Euonymus, Ficus, Fortunella, Hedera helix, Helicia, Jasminum nudiflorum, Ligustrum, Livistona, Maesa, Magnolia grandiflora, Mangifera indica, Musa paradisiaca, Myrica, Olea europaea, Palmae, Pandanus, Poncirus trifoliata, Populus, Prunus persica, Prunus, Psidium guajava, Rosa, Schefflera actinophylla, Smilax, Strelitzia reginae, Viburnum, Yucca.
Affected plant stages: vegetative, flowering, fruiting and post-harvest stages
Affected plant parts: leaves, fruits AONCITL2.jpg and occasionally stems
Biology and ecology
Aonidiella citrina reproduces sexually and is viviparous. It has been studied on satsuma and grapefruit in Izmir, Turkey (Onder, 1982), where it has three generations a year and overwinters mostly as the second instar stage. One generation takes 64 days in southern California (Nel, 1933).
Adult females of A. citrina produce species-specific sex pheromones to attract the winged adult males (Moreno et al., 1972a; Moreno et al., 1972b). The pheromones ((E)-3, 9-dimethyl-6-isopropyl-5, 8-decadienyl acetate), isolated from airborne collections (Gieselmann et al., 1979), have been found to differ in structure but exhibit identical chirality at C3 to the sex pheromones produced by A. aurantii (Roelofs et al., 1982). Male flight can be monitored using synthetic pheromones, which are commercially available.
Nel, 1933, found that fecundity appeared to be higher on the fruit than on the leaves; a single adult female produced 150 first instars on a lemon fruit. Most first instars settled to feed within 6 hours of emerging but some were active for up to 24 hours. Highest mortality occurred during the first instar. In California, A. citrina appeared to prefer Citrus growing in the more arid, warmer valleys and foothills of the interior, whereas A. aurantii prefers Citrus in the coastal regions. In Turkey, A. citrina has a development threshold of 14.8°C and a thermal constant of 449 day degrees (Onder, 1982).
Observations in the species card on A. aurtantii, on the importance of the control of certain ant species to maximise the effectiveness of natural enemies, are probably relevant to A. citrina also.
The dispersal phase of A. citrina is the first instar, or crawler, which has legs. Crawlers can walk up to perhaps 1 m, but can be distributed across much greater distances by wind, flying insects and birds and transport of infested plant material by man.
Symptoms
Aonidiella citrina usually attacks the leaves and fruit but rarely the bark (whereas A. aurantii occurs on all aerial parts of the plant). Heavy infestations may result in leaf discolouration, wilting and premature drop; dieback of apical twigs; and discoloured, stunted and pitted fruits, which fall prematurely or are unmarketable.
The small size, pale colour and sessile nature of A. citrina makes it difficult to detect unless it is present in large numbers. A. citrina can easily be confused with A. aurantii, which is one of the most commonly intercepted scale insects on imported Citrus fruit.
Economic impact
Aonidiella citrina is considered a damaging pest of Citrus fruits in some Citrus-growing regions. Fruits and leaves are attacked, but not usually branches or trunks. Heavily attacked fruits may lose their commercial value because of the unsightly pits and discoloration. Since A. citrina does not occur on the wood, overall damage is not as severe as that caused by A. aurantii (Gill, 1997). Aonidiella citrina was considered a major pest of Citrus in the San Joaquin Valley, California, USA, in the 1950s but is now rare there as a result of biological control. It has also been recorded as a non-specific pest of tea in Georgia (Dzhashi, 1970).
Phytosanitary risk
From its Asian origin, A. citrina has spread to various tropical and subtropical regions around the world. Some Citrus-producing countries worldwide are still free from this potentially important pest of Citrus. However, the threat is moderated by the following factors. Firstly, A. aurantii, which is now a common pest of Citrus in all major growing areas, appears to be a superior competitor and has even been replacing A. citrina in California, USA (DeBach et al., 1978). A. citrina may not be able to establish where A. aurantii is already present. Secondly, in Italy, where it was recently introduced, Longo et al., 1994, do not consider it as particularly threatening. This pest could therefore be less threatening for most subtropical countries that was origianally thought. In the Mediterranean area, it seems to have reached a stable status without specific measures. Finally, A. citrina has not been declared to be a quarantine pest by any regional plant protection organization, although it is listed as a quarantine pest by the European Union.
Detection and inspection methods
Direct inspections can be made of the leaves and fruit, aided by a x8 hand lens and a powerful torch if required, or by a dissection microscope in the laboratory. A. citrina does not normally infest bark, unlike A. aurantii. Look for yellowish or yellow-brown, flattened, circular scales about 1.5-2.0 mm in diameter (the adult females). Between these there are usually many immature scales which may be very small and pale (first instar) and others which grey to yellowish and intermediate in size.
Phytosanitary precautions
Importation of Citrus planting material is already prohibited or restricted by most Citrus-growing countries because of the risk of introduction of more important pests and diseases. Fruits should be subject to requirements such as area freedom, place of production freedom or treatment.
Natural enemies
Natural enemies are important for regulating populations of A. citrina, including Encarsia citrina which gave over 60% parasitism of A. citrina in Turkey (Onder, 1982) and Aphytis chrysomphali and Comperiella bifasciata in Australia (Hely et al., 1982). Longo et al. (1994) noted that the complex of natural enemies which controls A. aurantii in southern Italy (Encarsia citrina, Aphytis melinus and the introduced Chilocorus nigrita) is also effective against Aonidiella citrina.
Scale insect pheromones may act as kairomones to attract parasitoids.
Parasitoids:
- Aphytis aonidiae, attacking: nymphs. Greece, Hungary, Italy, Moldova, Russia, Spain, former Yugoslavia, Armenia, Cyprus, Georgia, Iran, Israel, Ukraine, USA (California), Argentina, Chile, Uruguay
- Aphytis chionaspis, attacking: nymphs, adults, in China; Japan. Introduced: USA; Australia; South Africa; Mediterranean Basin; Georgia
- Aphytis chrysomphali, attacking: nymphs, in Australia
- Aphytis lingnanensis, attacking: nymphs, in China, Taiwan and Japan. Introduced: USA (California), South Africa, Australia, Mexico, Argentina, Chile, Cyprus, Israel, Morocco
- Aphytis melinus, attacking: nymphs, in India, Pakistan. Introduced: USA (California), South Africa, Australia, Argentina, Chile, Cyprus, Israel, Italy, Morocco
- Comperiella bifasciata, attacking: nymphs, in India, China and Japan. Introduced: USA (California), South Africa, Swaziland, Australia, Mexico, Agrentina, Israel
- Encarsia aurantii, attacking: nymphs, adults, in Japan. Introduced to USA
- Encarsia citrina, attacking: nymphs, in Japan. Introduced to: USA; Australia; Mediterranean Basin; Turkey; Italy, Indonesia (Bali), Tahiti, Fiji, Cook Islands, Africa
- Encarsia lounsburyi, attacking: nymphs, adults in Brazil and Florida
- Encarsia perniciosi, attacking: nymphs, in China, Taiwan. Introduced: USA (California), Australia
Predators:
- Chilocorus kuwanae, attacking: nymphs, adults in China, Russian far east, Korea and Japan. Introduced to: Caucasus, Italy, India and USA
- Chilocorus nigrita, attacking: eggs, nymphs, adults, in Oriental region, Indonesia. Introduced to: southern Africa, Oman, Seychelles, American Samoa, Hawaii, Pohnpei and Mauritius and has spread naturally.
Distribution
See Aonidiella citrina distribution.
Microscopic examination of slide-mounted adult females is required for authoritative identification to species. Aonidiella citrina is very similar to A. aurantii and could be confused with A. inornata McKenzie, as all three species lack perivulvar pores. Aonidiella citrina does not normally infest bark, unlike A. aurantii. Aonidiella citrina possesses prevulvar apophyses but no scleroses AOCIP.jpg, whereas A. aurantii possesses both prevulvar apophyses and scleroses AOAUP.jpg; A. inornata lacks prevulvar apophyses and scleroses entirely AOINORP.jpg. The precise identity of A. inornata requires research, as its morphology is rather variable; Williams and Watson, 1988 remark that it may be a synonym of A. comperei McKenzie, 1938 or A. eremocitri McKenzie, 1937a (these species are discussed below). A key to separate five economically important species of Aonidiella in the tropics is given by Williams and Watson, 1988 (although this key does not include A. citrina). McKenzie, 1938, provided a key to separate the species of Aonidiella.
According to the literature, A. inornata AOINORP.jpg is fairly polyphagous on the leaves and fruit of hosts including species of Allamanda, Annesijoa, Areca, Artocarpus, Astronia, Barringtonia, Bischofia, Campnosperma, Carica, Citrus, Cocos, Cordyline, Cycas, Dracaena, Elettaria, Euphorbia, Hedyotis, Jasminum, Mangifera, Melaleuca, Metroxylon, Musa, Nerium, Pandanus, Piper, Plumeria and Vitis vinifera. It is known from India (Uttar Pradesh), Maldives, Indonesia (including Irian Jaya), Laos, West Malaysia, Sarawak, Brunei Darussalam, Thailand, China (Hainan, Hebei, Hong Kong, Inner Mongolia, Liaoning, Yunnan), South-East Asia, Taiwan, Japan, Okinawa, Philippines, Papua New Guinea, Australia (Queensland), Guam, Caroline Is, Marshall Is, Palau, Is, Pohnpei, Truk, Wake Is, Yap Is, Kiribati, Vanuatu, Fiji, Western Samoa, USA (Hawaii), Cayman Is, Puerto Rico and East Africa (Pemba I., Tanzania) (Takagi, 1969; Velasquez, 1971; Kawai, 1980; Nakahara, 1982; Williams and Watson, 1988; Watson et al., 1995; Danzig and Pellizzari, 1998; Tao, 1999; Heu, 2002; The Natural History Museum collection, London, UK). AOINORS.jpg
Aonidiella comperei McKenzie (false yellow scale) AOCOMPP.jpg and A. eremocitri McKenzie AONERP1.jpg are superficially similar to A. citrina but possess a few perivulvar pores on either side of the vulva, and lack the prevulvar apophyses that are present in A. citrina AOCIP.jpg. Aonidiella comperei AOCOMPS.jpg has been recorded from Barbados, Brazil (Alagôas, Guanabara, Paraíba, Pernambuco, Rio de Janeiro), Tanzania, China (Inner Mongolia), Taiwan, India (Lakshadweep Is, Maharashtra), Indonesia (Sulawesi), Maldive Is, Sri Lanka, Malaysia, Sarawak, Philippines, Mariana Is, Palau, Yap Is, Caroline Is, Truk Is, Marshall Is, Kiribati, Papua New Guinea and Australia (Queensland) on hosts from 8 plant families - Celastraceae, Compositae, Ebenaceae, Euphorbiaceae, Moraceae, Musaceae, Palmae and Rubiaceae (Borchsenius, 1966; Beardsley, 1966; Silva et al., 1968; Velasquez, 1971; Bennett and Alam, 1985; Williams and Watson, 1988; Watson et al., 1995; Claps et al., 2001a; The Natural History Museum collection, London, UK), including species of Annesijoa, Carica papaya, Citrus sinensis, Diospyros, Ficus, Melissa, Morinda, Musa, Pluchea, Rosa, Tamarindus and Vitis vinifera, and may have a wider host range. AONCOMP1.jpg
A. eremocitri AONERS.jpg has been recorded from Malaysia (Sarawak), Australia, Papua New Guinea, Solomon Is, Palau Is, Vanuatu and Fiji, on hosts from 9 plant families - Compositae, Ebenaceae, Euphorbiaceae, Moraceae, Musaceae, Orchidaceae, Palmae, Rubiaceae and Rutaceae including species of Barringtonia, Bischofia, Citrus, Cocos nucifera and Eremocitrus (Borchsenius, 1966; Beardsley, 1966; Bennett and Alam, 1985; Williams and Watson, 1988, Tao, 1999); it probably has a wider host range.
It is possible for inexperienced identifiers to confuse Aspidiotus macfarlanei Williams and Watson with Aonidiella citrina. Aspidiotus macfarlanei also develops a sclerotized, reniform body at maturity ASPMACS.jpg (Williams and Watson, 1988), but has marginal prepygidial macroducts and lacks paraphyses on the pygidium ASPMACP.jpg. Aonidiella citrina lacks marginal prepygidial macroducts, and possesses paraphyses AOCITP.jpg. Aspidiotus macfarlanei has been recorded from the Solomon Islands on Carica papaya and Cocos nucifera.
Comments
Aonidiella citrina originated in tropical Asia and has spread to various tropical and subtropical regions throughout the world; it occurs under glass in cold areas (Davidson and Miller, 1990). The precise distribution of A. citrina is uncertain due to difficulties in separating it from A. aurantii. A. aurantii is a common pest of Citrus found throughout the Mediterranean region and all major Citrus-growing areas of the world (CABI/EPPO, 1997; CABI/EPPO, 1998). Aonidiella citrina is not present in Argentina (Claps and Terán, 2001). All South Pacific island records of A. citrina are now all considered to be A. aurantii.
Europe
Cyprus: The Natural History Museum collection, London, UK
Italy: restricted to Calabria only (Longo et al., 1994; CABI/EPPO, 1997)
Former USSR: present, no further details (Tao, 1999)
Armenia: present, no further details (Nakahara, 1982)
Azerbaijan: present, no further details (CABI/EPPO, 1997)
Crimea: present, no further details (Nakahara, 1982)
Georgia: present, no further details (Nakahara, 1982)
Russia (Europe): restricted distribution (CABI/EPPO, 1997)
Southern Russia: restricted distribution; dominant scale species on Citrus in East Black Sea region, on coast in Krasnodar Territory (EPPO, 1999)
Transcaucasia: Georgia, under glass (CABI/EPPO, 1997; Danzig and Pellizzari, 1998)
Asia
Afghanistan: present, no further details (Ramaseshiah, 1985; CABI/EPPO, 1997)
Azerbaijan: present, no further details (CABI/EPPO, 1997)
Bangladesh: present, no further details (APPPC, 1987; CABI/EPPO, 1997)
China
Fujian: present, no further details (CABI/EPPO, 1997)
Guangdong: present, no further details (Tao, 1999)
Guangxi: present, no further details (Tao, 1999)
Hebei: present, no further details (CABI/EPPO, 1997)
Hong Kong: present, no further details (CABI/EPPO, 1997)
Hubei: present, no further details (Tao, 1999)
Hunan: present, no further details (Tao, 1999)
Inner Mongolia: present, no further details (Tao, 1999)
Jiangsu: present, no further details (CABI/EPPO, 1997)
Jiangxi: present, no further details (CABI/EPPO, 1997)
Qinghai: present, no further details (CABI/EPPO, 1997)
Sichuan: present, no further details (Tao, 1999)
Taiwan: present, no further details (CABI/EPPO, 1997)
Xizhang: present, no further details (Tao, 1999)
Yunnan: present, no further details (Tao, 1999)
Zhejiang: present, no further details (Tao, 1999)
India: present, no further details (Tao, 1999)
Andhra Pradesh: present, no further details (CABI/EPPO, 1997)
Delhi: present, no further details (CABI/EPPO, 1997)
Karnataka: present, no further details (CABI/EPPO, 1997)
Maharashtra: present, no further details (CABI/EPPO, 1997)
Orissa: present, no further details; Natural History Museum collection, London, UK
Uttar Pradesh: present, no further details (CABI/EPPO, 1997)
Indonesia
Irian Jaya: present, no further details (EPPO, 1999)
Iran: present, no further details (Seghatoleslami, 1977; Abivardi, 2001)
Japan: present, cannot read any further details (Kawai, 1980; Tao, 1999)
Honshu: present, no further details (CABI/EPPO, 1997)
Korea, Republic of: present, no further details (APPPC, 1987; CABI/EPPO, 1997)
Malaysia
Sabah: present, no further details (CABI/EPPO, 1997)
Sarawak: present, no further details (CABI/EPPO, 1997)
Nepal: present, no further details (Nakahara, 1982)
Pakistan: present, no further details (CABI/EPPO, 1997)
Philippines: present, no further details (Velasquez, 1971; CABI/EPPO, 1997)
Saudi Arabia: present, no further details (CABI/EPPO, 1997)
Taiwan: widespread (Takagi, 1969)
Thailand: present, no further details (CABI/EPPO, 1997)
Turkey: restricted distribution (Bozan and Yildrim, 1992; CABI/EPPO, 1997)
Yemen: present, no further details (CABI/EPPO, 1997)
Africa
Benin: present, no further details (CABI/EPPO, 1997)
Cameroon: present, no further details (CABI/EPPO, 1997)
Congo: present, no further details (CABI/EPPO, 1997)
Côte d'Ivoire: present, no further details (CABI/EPPO, 1997)
Ethiopia: present, no further details (CABI/EPPO, 1997)
Gabon: present, no further details (CABI/EPPO, 1997)
Guinea: present, no further details (CABI/EPPO, 1997)
Libya: present, no further details (CABI/EPPO, 1997)
Madagascar: present, no further details (CABI/EPPO, 1997)
Mali: widespread (Vilardebo, 1974; CABI/EPPO, 1997)
Mauritius: present, no further details (CABI/EPPO, 1997)
Niger: present, no further details (CABI/EPPO, 1997)
Senegal: present, no further details (CABI/EPPO, 1997)
South Africa: absent, reported but not confirmed (EPPO, 1999)
St Helena: present, no further details (CABI/EPPO, 1997)
Tanzania: restricted distribution (CABI/EPPO, 1997)
Zanzibar: present, no further details (CABI/EPPO, 1997)
Uganda: present, no further details (Tao, 1999)
Yemen (southern): present, no further details (Nakahara, 1982)
Western Hemisphere
Argentina
Corrientes: present, no further details (CABI/EPPO, 1997)
Misiones: present, no further details (CABI/EPPO, 1997)
Chile: present, no further details (CABI/EPPO, 1997)
Tarapacá: present, no further details (Claps et al., 2001a)
Valparaiso: present, no further details (Claps et al., 2001a)
Jamaica: present, no further details (Tao, 1999)
Mexico: Nuevo Leon (Miller, 1996; CABI/EPPO, 1997)
Nicaragua: present, no further details (Tao, 1999)
North America: present, no further details (Danzig and Pellizzari, 1998)
South America: present, no further details (Danzig and Pellizzari, 1998)
Trinidad: present, no further details (CABI/EPPO, 1997)
USA
California: once widespread, becoming rare (Gill, 1997)
Florida: present, no further details (Gill, 1997)
Texas: present, no further details (Gill, 1997)
Oceania
Australia: present, no further details (Tao, 1999; Danzig and Pellizzari, 1998)
New South Wales: present, no further details (CABI/EPPO, 1997; CSIRO, 2001)
South Australia: present, no further details (CABI/EPPO, 1997; CSIRO, 2001)
Victoria: present, no further details (CABI/EPPO, 1997; CSIRO, 2001)
Western Australia: present, no further details (CABI/EPPO, 1997; CSIRO, 2001)