(Comstock, 1883)
Diagnosis
Scale cover of adult female mussel-shaped, up to 2.5 mm long; slightly convex, brown or brown-black with a paler margin, moderately convex and often with a distinct longitudinal dorsal ridge; with brown-yellow terminal exuviae UNCITL1.jpg and UNCITL4.jpg . Scale cover of male smaller than that of female, white, elongate oval, with three longitudinal ridges and yellow-brown terminal exuviae (Miller and Davidson, 1990) UNCITL6.jpg . The male scale covers often form conspicuous groups on bark - hence the common name, citrus snow scale UNCITL2.jpg and UNCITL5.jpg .
Body of slide-mounted adult female membranous, elongate, more than twice as long as wide UNCITS.jpg . Pygidium with median lobes not zygotic, with a pair of setae present between their bases; dorsum of pygidium with 60-75 scattered dorsal macroducts present UNCITP.jpg .
Detailed morphological descriptions, illustrations and keys to Unaspis are provided by Balachowsky, 1954; Ferris, 1937; and Williams and Watson, 1988.
Host range
Unaspis citri is fairly polyphagous, attacking plant species belonging to 9 genera in 7 plant families (Davidson and Miller, 1990). The main hosts of economic importance are Citrus spp., especially orange, but the insect is also recorded on a wide range of other crops, mostly fruit crops and ornamentals. Hosts include species of: Ananas comosus, Annona muricata, Artocarpus heterophyllus, Capsicum, Citrus spp., Cocos nucifera, Euonymus, Fortunella, Hibiscus, Mangifera indica, Musa, Olea europaea, Osmanthus, Palmae, Persea americana, Poncirus, Psidium guajava, Rollinia, Severinia and Tillandsia.
Affected plant stages: vegetative growing, flowering, fruiting and post-harvest stages
Affected plant parts: usually on the trunk and main limbs UNCITL5.jpg , but occasionally on leaves UNCITL6.jpg and fruits
Biology and ecology
Unaspis citri reproduces sexually and produces several overlapping generations a year; populations tend to peak in late autumn. The life cycle takes 10-12 weeks to complete in summer but longer during cooler weather. Each female can produce up to 169 first instars (over a period of 146 days); the average number of offspring per female is about 80 (Hely et al., 1982). Laboratory studies of the population dynamics of U. citri showed that the net reproductive rate, intrinsic rate of increase and finite rate of increase were higher on orange than on lemon. The longevity of female scales on orange was approximately 13 weeks compared to 17 weeks on lemon (Fernandez and Garcia, 1988). Population studies in Colombia have shown that at any given time, 86.5 to 95.5% of U. citri are not feeding and that 43.9 - 79.3% of first instars are males, which cease to feed after the second moult (Mosquera, 1979). Two to three generations per year have been recorded in the former USSR (Tikhonov, 1966) and Japan (Borchsenius, 1950), while four generations per year occur in typical Citrus-growing areas (Brooks, 1977).
Like other diaspidids, the main dispersal stage of U. citri is the mobile first instar, which also may be naturally dispersed by wind and animals. First instars are most abundant during late spring, summer and autumn. Once a feeding site has been selected, the insect becomes sessile and is not naturally dispersed (Hely et al., 1982). However, it is readily carried on consignments of plant material and fruit.
Unaspis citri is a tropical species that thrives in humid tropical conditions; in West Africa it does not occur where there is a dry season (Vilardebo, 1974). In Australia (Queensland and New South Wales) it is confined to the non-irrigated humid coastal regions and does not occur in the semi-arid, irrigated Citrus-cultivation areas inland (Maelzer, 1979).
Symptoms
Infestations of U. citri usually occur on the trunk and main limbs of trees under ten years old. Heavily infested bark becomes dark, dull, and hard, appears tight and subsequently splits (Claps et al., 2001a). Weakened limbs and twigs become infected with fungi and may be subsequently attacked by wood-boring insects. Heavy infestations spread to the twigs, leaves and fruit. The toxicity of injected saliva results in yellow spotting and development of necrotic areas around each feeding site on the undersides of leaves, which drop prematurely; discolouration of fruit; dieback of twigs; and weakening and eventual death of branches.
Economic impact
Unaspis citri is one of the principal pests of Citrus spp. in many of the Citrus-growing regions of the world. It infests the trunk, branches and small shoots, causing serious damage to orchards due to leaf drop and rapid dieback. Bark splitting on Citrus was reported from Fiji by Swaine, 1971; from Niue by Meister, 1975; and from Papua New Guinea by Brough, 1986. Relatively small numbers of scales can cause damage, due to the phytotoxic saliva they inject while feeding. There are records of U. citri as a major pest of Citrus in several countries in the South Pacific region (Williams and Watson, 1988). In 1976, it was estimated that U. citri caused an annual loss on Citrus in Florida of US$7 million (Kosztarab, 1990). Crouzel, 1973, lists U. citri as a pest in Argentina.
Detection and inspection methods
If present, large groups of white male scale covers on trunk UNCITL5.jpg , stems and leaves UNCITL6.jpg are conspicuous (hence the common name of Citrus snow scale). However, the small size, dark colour and sessile nature of the female scales UNCITL4.jpg makes them difficult to detect unless they are present in large numbers. Bark, stems, leaves and fruit therefore should be examined closely in good light. On Citrus fruit, female U. citri can be confused with the common Lepidosaphes spp. or easily overlooked as dirt particles.
Phytosanitary risk and regulatory control
Unaspis citri is listed in the European Community Plant Health Directive Annex IIAI and is a quarantine pest on Citrus, Fortunella and Poncirus spp. (other than fruit and seeds). Unaspis citri appears on the quarantine pest list of Russia and is under renewed consideration by EPPO as a potential A1 quarantine pest. The cryptic female scales are difficult to detect at plant quarantine inspection.
Importation of Citrus plants for planting from countries where U. citri occurs should be prohibited. Fruits should be subject to requirements such as area freedom, place of production freedom or treatment.
Unaspis citri is a more tropical species than the closely related U. yanonensis, and has less of a tendency to attack fruits than U. yanonensis.
Natural enemies
Important natural enemies of U. citri include the hymenopterous parasitoids Aphytis lingnanensis and Aspidiotiphagus lounsburyi and in Australia, a predatory caterpillar, Batrachedra sp. (for a complete list see Waterhouse and Norris, 1987). In Australia, Batrachedra sp. causes spectacular reductions in the number of scales whenever pest populations become dense (Hely et al., 1982). Existing biological control agents include Aphytis lingnanensis used in Florida (USA), the Solomon Islands and Cuba, and Aspidiotiphagus lounsburyi in Cuba. See Rosen, 1990a, for a discussion and further references to the natural enemies of Diaspididae.
Parasitoids:
- Aphytis lingnanensis, attacking: nymphs, in China, Taiwan and Japan. Introduced: USA (California), South Africa, Australia, Mexico, Argentina, Chile, Cyprus, Israel, Morocco
- Aphytis yanonensis, attacking: nymphs, adults, in USA (introduced)
- Arrhenophagus chionaspidis, attacking: nymphs, adults, in Argentina, Brazil, Guyana
- Encarsia aurantii, attacking: nymphs, adults, in USA
- Encarsia citrina, attacking: nymphs, in Japan. Introduced to: USA; Australia; Mediterranean Basin; Turkey; Italy, Indonesia (Bali), Tahiti, Fiji, Cook Islands, Africa
- Encarsia herndoni, attacking: nymphs, adults, in Argentina
- Encarsia lounsburyi, attacking: nymphs, adults, in Vanuatu, Australia, Argentina, Trinidad, Venezuela; Introduced: USA, Cuba
- Encarsia perniciosi, attacking: nymphs, in China, Taiwan. Introduced: USA (California), Australia
Predators:
- Batrachedra arenosella, attacking: nymphs, adults, in Australia
- Hemisarcoptes malus, attacking: nymphs, adults, in USA
Pathogens:
- Fusarium sp., attacking: nymphs, adults, in Australia
- Myriangium duriaei, attacking: nymphs, adults, in Cuba, Florida, St. Lucia
- Nectria aurantiicola, attacking: nymphs, adults, in Colombia
- Nectria flammea, attacking: nymphs, adults, in Guyana
- Verticillium lecanii, attacking: nymphs, adults, in Venezuela
Distribution
See Unaspis citri distribution.
Microscopic examination of slide-mounted adult females is required for authoritative identification to species.
On Citrus fruit, the female scales of U. citri can be confused with the common Lepidosaphes spp. However, adult female U. citri scale coversoften have a distinct longitudinal dorsal ridge UNCITL.jpg that is absent in those of Lepidosaphes spp LEPBEL.jpg. Also, male scale covers of U. citri are white, felted, elongate oval in shape with three longitudinal ridges; those of Lepidosaphes spp. LEBEL1.jpg are mussel-shell shaped, purplish or brown and similar in appearance to, but smaller than, the female scales.
Unachionaspis bambusae (Cockerell) UNABS.jpg is a species not included in the key, which could be mistaken for Unaspis citri. However, Unachionaspis bambusae is found only on species of bamboo; the female scale cover is white UNCHIBL2.jpg ; the dorsal macroducts are arranged in segmental rows, and there are perivulvar pores present UNABP.jpg. Unaspis citri occurs on species of Citrus and other broad-leaved hosts, never on bamboo; the female scale cover is dark brown UNCITL1.jpg ; the dorsal macroducts are scattered and perivulvar pores are absent UNCITP.jpg. Unachionaspis bambusae is known from former USSR (Far East), China (Anhui, Jiangsu, Fujian, Sakhalin) and Japan (Honshu) on the lower leaf surfaces of species of Phyllostachys and Sasa (Tao, 1999; Danzig and Pellizzari, 1998; Kawai, 1980). The male scale cover is much smaller and narrower than that of the female, parallel sided, with longitudinal ridges UNCHIBL1.jpg . This species is a pest of bamboo in China (Anhui), where there are three generations per year (Wu, 1981). See also genus Unachionaspis, Background.
Unaspis euonymi (Comstock) (euonymus scale, spindle-berry scale, cochenille du fusain, piojo de los evónimos, cochinilla blanca alargada de los evónimos) UNEUL2.jpg and UNEUL5.jpg could be misidentified as U. citri but differs by lacking perivulvar pores UNEUP.jpg, and the prosoma remains membranous throught life UNEUS.jpg. In U. citri, perivulvar pores are present UNCITP.jpg, and the prosoma becomes sclerotized at maturity UNCITS.jpg. Unaspis euonymi is known from China (Guangdong, Hong Kong, Inner Mongolia, Jiangsu, Shandong, SE China), Japan (Hokkaido, Honsu, Kyushu, Shikoku), Korea, Austria, Bulgaria, England, former USSR (Armenia, Azerbaijan, Caucasus, Crimea, Georgia, Krasnodar Territory, Ukraine, Uzbekistan), France, Germany, Greece, Hungary, Italy, Poland, Sardinia, Sicily, Malta, Portugal, Romania, Spain (mainland and Canary Is), Switzerland, former Yugoslavia, Turkey, Israel, Algeria, Morocco, Canada (British Colombia), Egypt, Iran, Israel, China, Japan, Korea, South-East Asia, Canada, USA (Alabama, Arkansas, California, Connecticut, Delaware, District of Colombia, Florida, Georgia, Illinois, Indiana, Kentucky, Louisiana, Maryland, Massachussetts, Michigan, Mississippi, Missouri, New England, New Hampshire, New Jersey, New Mexico, New York, North Carolina, Ohio, Oklahoma, Pennsylvania, Rhode Island, South Carolina, Tennessee (under glass), Texas, Virginia, Wisconsin and West Virginia), Mexico, Honduras, Argentina (Buenos Aires, Córdoba, Cuyo, Jujuy, Santa Fe) and Bolivia on aerial parts (usually stems and leaves) of hosts from 18 genera in 7 plant families, although it is rarely found on hosts other than Euonymus (Squire, 1972a; Davidson and Miller, 1990; Amparo Blay Golcoechea, 1993; Labanowski and Soika, 1997; Schmutterer, 1998). Unaspis euonymi has been recorded on aerial parts of species of Buxus, Celastrus, Citrus, Daphne, Euonymus, Fraxinus, Hedera, Hibiscus, Ilex, Jasminum, Lagerstroemia, Ligustrum, Lonicera, Magnolia, Olea, Pachysandra, Pachystigma, Prunus, Syringa and Viscum (CIE, 1970a; Seghatoleslami, 1977; Kawai, 1980; Nakahara, 1982; Carnero Hernandez and Perez Guerra, 1986; Kosztarab and Kozár, 1988; Davidson and Miller, 1990; Amparo Blay Golcoechea, 1993; Kozár et al., 1994; Longo et al., 1995; Miller, 1996; Gill, 1997; Danzig and Pellizzari, 1998; Tao, 1999; Foldi, 2001; Claps et al., 2001a). The species probably originated in eastern Asia (Longo et al., 1995). It is a major pest of Euonymus (Davidson and Miller, 1990); bark may become distorted and leaves may develop chlorotic spotting as a result of infestation (Kosztarab, 1990; Kosztarab, 1996) and unchecked infestations can kill Euonymus japonica (Davidson and Miller, 1990; Gill, 1997). In Hungary, it is one of the most important scale insect pests of ornamental trees and shrubs (Ripka, 1999). Danzig and Pellizzari, 1998, describe this species as a dangerous pest in the Palaearctic region, and Foldi, 2001, lists it as an occasional pest in France. In life, adult female scale cover 1.5-2.2 mm long, mussel-shaped, slightly convex, dark brown with yellowish-brown terminal exuviae; male scale cover elongate, white, strongly tricarinate, with brown-yellow terminal exuviae. The males are very common and easily seen. Exposed body of living female orange yellow (Kosztarab and Kozár, 1988).There are 2-3 generations per year and overwintering is mainly as adult females (Davidson and Miller, 1990). Each female lays 30-50 eggs (Kosztarab and Kozár, 1988). This species is a 'B'-rated pest in California (Gill, 1997). The extensive literature on U. euonymi is indicative of the importance of this insect. Colonies UNEUL1.jpg ; UNEUL4.jpg ; male and female scale covers UNEUL3.jpg ; male scale covers UNEUL6.jpg
Comments
Unaspis citri originated in Asia and has spread widely in other tropical and subtropical regions. It is now found in North, Central and South America, Africa and Oceania (CIE, 1962; CABI/EPPO, 1998a) but has not been recorded from much of Europe.
In spite of records in the past (CIE, 1962; EPPO, 1999), U. citri is not present in New Zealand now (Charles and Henderson, submitted). The species was recorded from the Azores in the 1920s, but there have been no records since (CIE, 1962; EPPO, 1999).
Europe
Greece: present, no further details (Nakahara, 1982)
Malta: present, no further details (EPPO, 1999)
Portugal: present, no further details (Nakahara, 1982)
Spain: present, no further details (Nakahara, 1982)
Asia
Brunei Darussalam: The Natural History Museum collection, London, UK
China
Guangdong: present, no further details (Tao, 1999)
Hong Kong: present, no further details (Tao, 1999)
Hubei: present, no further details (CIE, 1962)
North China: present, no further details (Tao, 1999)
Sichuan: present, no further details (Tao, 1999)
Indonesia
Java: present, no further details (CIE, 1962)
Japan: present, no further details (Danzig and Pellizzari, 1998; Tao, 1999)
Malaysia
West Malaysia: present, no further details (CIE, 1962)
Sabah: The Natural History Museum collection, London, UK
Philippines: present, no further details (Nakahara, 1982)
Singapore: present, no further details (EPPO, 1999; Tao, 1999)
Syria: present, no further details (Danzig and Pellizzari, 1998)
Thailand: present, no further details (Nakahara, 1982)
Vietnam: present, no further details (CIE, 1962; 2000 data from S. Kawai photographs)
Yemen: widespread on lime (EPPO, 1999)
Africa
Benin: present, no further details (CIE, 1962)
Cameroon: present, no further details (EPPO, 1999)
Congo Democratic Republic: present, no further details (CIE, 1962; Nakahara, 1982)
Côte d'Ivoire: present, no further details (CIE, 1962)
Egypt: present, no further details (Danzig and Pellizzari, 1998)
Gabon: present, no further details (EPPO, 1999)
Guinea: present, no further details (CIE, 1962)
Liberia: present, no further details (Nakahara, 1982)
Madagascar: present, no further details (Nakahara, 1982)
Mali: present, no further details (Nakahara, 1982)
Mauritius: present, no further details (Williams and Williams, 1988)
Niger: present, no further details (EPPO, 1999)
Nigeria: present, no further details (CIE, 1962)
Senegal: present, no further details (EPPO, 1999)
Sierra Leone: present, no further details (CIE, 1962)
Togo: present, no further details (CIE, 1962)
Western Hemisphere
Antigua and Barbuda: present, no further details (CIE, 1962)
Argentina: frequent on Citrus (Claps et al., 2001a)
Corrientes: present, no further details (CIE, 1962)
Entre Rios: present, no further details (Claps et al., 2001a)
Misiones: present, no further details (CIE, 1962)
Paraná Delta: present, no further details (CIE, 1962)
Salta: present, no further details (Claps et al., 2001a)
Tucumán: present, no further details (Claps and Terán, 2001; Claps et al., 2001a)
Barbados: present, no further details (Bennett and Alam, 1985)
Belize: The Natural History Museum collection, London, UK
Bermuda: common (Hodgson and Hilburn, 1991)
Bolivia: present, no further details (Squire, 1972a)
Brazil: widely distributed (Claps et al., 2001a)
Guanabara: present, no further details (Silva et al., 1968)
Mato Grosso: present, no further details (Claps et al., 2001a)
Rio Grande do Sul: present, no further details (CIE, 1962; Claps et al., 2001a)
Rio de Janeiro: present, no further details (CIE, 1962; Claps et al., 2001a)
Sao Paulo: present, no further details (CIE, 1962; Claps et al., 2001a)
British Virgin Islands: present, no further details (CIE, 1962)
Chile
Tarapacá: present, no further details (Claps et al., 2001a)
Colombia: present, no further details (CIE, 1962; Mosquera, 1973; Kondo, 2001)
Costa Rica: The Natural History Museum collection, London, UK
Cuba: present, no further details (CIE, 1962)
Dominica: present, no further details (CIE, 1962)
Dominican Republic: present, no further details (CIE, 1962)
Ecuador: present, no further details (CIE, 1962)
El Salvador: present, no further details (EPPO, 1999)
Grenada: present, no further details (CIE, 1962)
Guadeloupe: present, no further details (CIE, 1962)
Guyana: present, no further details (CIE, 1962)
Haiti: present, no further details (CIE, 1962)
Honduras: present, no further details (EPPO, 1999)
Jamaica: present, no further details (CIE, 1962)
Mexico: present, no further details (Davidson and Miller, 1990; Miller, 1996)
Montserrat: present, no further details (CIE, 1962)
Nevis: present, no further details (CIE, 1962)
Panama: present, no further details (CIE, 1962)
Paraguay: present, no further details (CIE, 1962)
Peru: present, no further details (CIE, 1962)
Puerto Rico: present, no further details (CIE, 1962)
St Lucia: present, no further details (CIE, 1962)
St Vincent and the Grenadines: present, no further details (CIE, 1962)
Trinidad and Tobago: present, no further details (CIE, 1962)
Uruguay: present, no further details (CIE, 1962)
USA
California: present, no further details (CIE, 1962)
Florida: present in most counties (Dekle, 1976; Miller, 1996)
Georgia: present, no further details (EPPO, 1999)
Louisiana: present, no further details (Howard and Oliver, 1985; Miller, 1996)
United States Virgin Islands: present, no further details (CIE, 1962; EPPO, 1999)
Venezuela: present, no further details (CIE, 1962)
Oceania
Australia: present, no further details (Davidson and Miller, 1990)
New South Wales: restricted distribution (CSIRO, 2001)
Northern Territory: The Natural History Museum collection, London, UK
Queensland: widespread (CSIRO, 2001)
South Australia: present, no further details (EPPO, 1999)
Victoria: present, no further details (EPPO, 1999)
Caroline Is: The Natural History Museum collection, London, UK
Cook Islands: present (Williams and Watson, 1988)
Fiji: present (Williams and Watson, 1988)
Kiribati: present (Williams and Watson, 1988)
Marshall Is, Lora: The Natural History Museum collection, London, UK
New Caledonia: present (Williams and Watson, 1988)
Niue: present, no further details (Williams and Watson, 1988)
Papua New Guinea: present (Williams and Watson, 1988)
Pohnpei, damaging Citrus in some areas (Nakahara, 1982)
Samoa: present, no further details (Williams and Watson, 1988)
Solomon Islands: present (Williams and Watson, 1988)
Tonga: present (Williams and Watson, 1988)
Truk Is: present, no further details (Nakahara, 1982)
Vanuatu: present (Williams and Watson, 1988)
Wallis I.: present, no further details (CIE, 1962)
Western Samoa: present (Williams and Watson, 1988)