Aphis craccivora
(groundnut aphid)

Preferred Common Name

• groundnut aphid

Other Scientific Names

• Aphis atronitens Cockerell, 1903
• Aphis beccarii del Guercio, 1917
• Aphis cistiella Theobald, 1923
• Aphis citricola del Guercio, 1917
• Aphis dolichi Montrouzier, 1861
• Aphis hordei del Guercio, 1913
• Aphis isabellina del Guercio, 1917
• Aphis kyberi Hottes, 1930
• Aphis laburni Theobald
• Aphis leguminosae Theobald, 1915
• Aphis loti Kaltenbach, 1862
• Aphis mimosae Ferrari, 1872
• Aphis oxalina Theobald, 1925
• Aphis papilionacearum van der Goot, 1918
• Aphis robiniae Macchiati, 1885
• Doralida loti (Kaltenbach)
• Doralina craccivora (Koch)
• Doralina salsolae Börner, 1940
• Doralis laburni (Kaltenbach)
• Doralis meliloti Börner, 1939
• Doralis robiniae (Macchiati)
• Pergandeida craccivora Koch
• Pergandeida loti (Kaltenbach)
• Pergandeida robiniae (Macchiati)

International Common Names

• English: African bean aphid; bean aphid; black legume aphid; black lucerne aphid; cowpea aphid; lucerne aphid; oriental pea aphid
• Spanish: afido del mata-ratón; pulgón negro (leguminosas, alfalfa, fréjol, caupi)
• French: puceron de l'arachide; puceron noir (lucerne, gourgane); puceron oriental du pois

Local Common Names

• Denmark: vikkebladlus
• Germany: kundebohnen-blattlaus; robinien-blattlaus; schwarze klee-blattlaus
• Iran: schatte schabdar
• Israel: knimat hakitnyiot
• Japan: mame-aburamusi
• Netherlands: grijszwarte bladluis; zwarte wikkeluis

EPPO code

• APHICR (Aphis craccivora)

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Sternorrhyncha
•                             Unknown: Aphidoidea
•                                 Family: Aphididae
•                                     Genus: Aphis
•                                         Species: Aphis craccivora

A. craccivora was first described by Koch in 1854. There are a number of synonyms in the literature (Eastop and Hille Ris Lambers, 1976).

A. craccivora is a relatively small aphid. Apterous viviparous females have a shiny black or dark brown body with a prominent cauda and brown to yellow legs. Immatures are slightly dusted with wax, adults without wax. Six-segmented antennae. Distal part of femur, siphunculi and cauda black. Apterae 1.4-2.2 mm.

Alate viviparous A. craccivora females have abdomens with dorsal cross bars. Alatae 1.4-2.1 mm (Blackman and Eastop, 2000).

Groundnut plants take on a bushy appearance due to attack by A. craccivora and infection with rosette virus. Rosette may take two forms, chlorotic rosette (white patches with green veins on young leaves and short internodes) and green rosette (darker appearance with stunting of leaflets and branches).

Introduction

A. craccivora is a cosmopolitan species with a worldwide distribution; abundant in subtropical and tropical regions, and in the Mediterranean. It is one of the commonest aphid species in the tropics.

A. craccivora is mainly found on plants in the Leguminosae. It is a major economic pest of groundnut and cowpea, particularly in the tropics, and a significant pest of mungbean (Vigna radiata), pigeonpea (Cajanus cajan), chickpea (Cicer arietinum), field and green beans (Vicia spp. and Phaseolus spp.), lupins (Lupinus angustifolius), lentil (Lens esculenta) and lucerne (Medicago sativa). It is also a minor pest on a range of other leguminous crops, and also some non-leguminous crops, such as cotton and citrus. There is little in the way of published information on financial losses caused by A. craccivora. However, it is an important pest in economic terms in groundnuts, cowpeas and a range of other leguminous crops. Crop losses caused by A. craccivora are due to direct feeding damage and to indirect damage, chiefly via the transmission of plant viruses.

Direct Feeding Damage

Direct damage caused by A. craccivora occurs on the seedling, vegetative and flowering stages of plants. Aphids prefer to feed on young leaves, shoots, flowers and immature seed pods. It is when aphid colonies concentrate on the growing tips of plants in the spring that the highest yield losses due to direct damage occur.

Groundnuts
A. craccivora is the most important pest of groundnuts in the tropics. Sap removal and physiological reactions of plants to aphid feeding cause direct damage. The removal of sap weakens the plant, causing poor and stunted growth, leaf curling and distorted leaf growth, wilting and reduced resistance to drought conditions, all resulting in yield losses. Damage due to irritants and toxins, produced by aphid feeding on the leaves and growing points, manifests itself in necrosis and other adverse reactions. A brown necrosis may be induced in groundnuts, for example, while disturbances in fruiting and a reduction in the root system can occur. Direct feeding damage on groundnuts by large numbers of aphids can also result in partial sterility of plants (Mayeux, 1984).

A. craccivora is probably the most injurious insect species of groundnut throughout Africa (Mayeux, 1984; Attia et al., 1986; Tarimo and Karel, 1987; Wightman and Wightman, 1994). The presence of aphids, known not to be carrying plant viral diseases, caused groundnut yields to drop by about 48%, compared with controls, in a study in Niger. The effects of aphid feeding became insignificant after the 42nd day of seedling growth, compared with controls, by which time 73% of the pods had been formed. The economic damage due to aphids varies with the stage of plant development, with most damage caused if aphids infest the growing points of groundnut early in the plant's development (Mayeux, 1984). In southern Africa, groundnut yields of 0.6-0.7 tons dry pods/ha are typical, well below what can be achieved on research farms (for example, 2.0 t/ha), mainly because of losses due to crop pests and diseases (Wightman and Wightman, 1994).

In Asia, A. craccivora appears in groundnut early in the rainy season, when it can cause considerable direct feeding damage. Yield losses of ca 16% were recorded in groundnut in India due to a complex of insect pests, the predominant one being A. craccivora (Jagtap et al., 1984).

Cowpeas and other crops
A. craccivora is the most important aphid pest of cowpeas worldwide. Direct feeding damage is due to the removal of sap from leaves, pods, seeds and other aerial plant parts. Symptoms include plant stunting and seed shrivelling. In tropical regions, direct feeding damage can result in large yield reductions.

In greenhouse studies on cowpea seedlings in Nigeria, infestation with A. craccivora at the young and mid-fill pod stage caused significantly more pod shrivelling compared with uninfested pods. Infestation at the mature pod stage alone caused relatively little pod shrivelling. However, all experimental levels of infestation caused significant reductions in seed yield, irrespective of the age of the pod (Ofuya, 1989). The use of resistant cowpea varieties, combined with the presence of natural enemies, can be an effective means of pest control in Nigeria (Ofuya, 1995; Bottenberg et al., 1998).

In field and greenhouse studies in Kenya on cowpea, the influence of the duration of infestation by A. craccivora on aphid-resistant (ICV-12) and aphid-susceptible (ICV-1) cultivars was compared with uninfested controls. Significant interactions were found between cultivar and duration of infestation for plant yields, quantified as pods per plants and seeds per pod. Reductions in seeds per pod were significantly reduced by aphid infestations of 7 days or more. The cultivar selection and aphid density at initial infestation were the major factors on cowpea growth and yield (Annan et al., 1995, 1996). In further studies, it was found that fertilizer application and cultivar selection were both important for cowpea growth and yield, as well as aphid population dynamics and bionomics. Aphid counts were higher in all fertilizer treatments compared with untreated controls. Cultivar selection was the most important factor determining yield, with aphid-resistant cultivars giving best yields. With susceptible cultivars, fertilizer application in some cases counteracted the adverse effects of A. craccivora feeding, but in other cases actually aggravated the plant growth deformities and yield reductions caused by aphids (Annan et al., 1997).

Infestations of A. craccivora on cowpeas produced deleterious effects on plant physiology, manifested in reduced growth (quantified by leaf height, leaf area growth rate and plant height) and losses in yield (Annan et al., 1995). In Canadian laboratory studies, short-term feeding was shown to significantly alter carbon dioxide exchange and photoassimilate partitioning. If infestation lasted 10 days or more, significant reductions in plant growth and respiration resulted. If infestations were terminated, plants could compensate for aphid-induced physiological changes (Hawkins et al., 1987, 1988). Direct feeding damage caused by inoculation of cowpea with A. craccivora, in a Chinese study, resulted in a reduction in plant height (to 41.9% of the controls), reduction in the green leaf area index from the 7th day after inoculation, and delayed production of harvestable pods by 30 days (Chang and Thrower, 1981).

In Pakistan, A. craccivora infestations ranged from 14 to 76% on chickpea, and from 11 to 100% on lentil, with indigenous varieties exhibiting the greatest levels of resistance (Mushtaq, 1977). In a study of the efficacy of synthetic pyrethroid pesticides on greengram (Vigna radiata) in Assam, India, against A. craccivora, the yield in infested and untreated field plots was 2.52 q/ha. This compared with yields of 6.39-11.57 q/ha in plots treated with eight pyrethroid insecticides. Even in untreated plots, however, aphid populations declined toward the end of the study, probably due to rising temperature and maturity of the crop (Borah, 1996).

A. craccivora was reported to be the most damaging pest of cowpeas in Egypt, particularly early in the growing season with aphids migrating from other food plants (Attia et al., 1986). Untreated faba bean fields in Egypt suffered slight to heavy damage due to direct feeding by A. craccivora (Bishara et al., 1984). The aphid is also a significant pest of mungbean in Egypt (Farghali et al., 1996).

In pasture grasses, A. craccivora can reach large population levels, causing direct feeding damage. Large colonies have been reported in the inflorescences of lucerne in Russia at the beginning of the flowering period, with infestation of plants sometimes reaching 60-70% (Keston, 1975). A. craccivora is also an important pest of cotton in the Zaravshan valley of Uzbekistan (Khushbaktov, 1995).

The economic injury level (EIL) of A. craccivora has been calculated as 10-16 aphids/plant on green gram (cv. AAU 34) in India (Sarma et al., 2000), 10.82 aphids/plant on black gram (cv. T-9) in India (Deka and Dutta, 2001) and 8.6 aphids/plant on faba bean in Egypt, depending on the market price of bean and control cost during the season (Abdou et al., 2012).

Factors Affecting Yield Loss

Environmental factors affect yield losses due to direct feeding damage, which is related to aphid population development. The optimal development time of A. craccivora in experimental studies occurs at around 65% relative humidity and in temperatures between 24-28.5°C (Mayeux, 1984).

In a study on field beans (Vicia faba) in Hungary during 1986 and 1987, A. craccivora was common and of economic importance, with 22.3 aphids/plant on average recorded in 1986. In this year, rapid population increase was attributed to relatively high temperatures (16.8-17.6°C) in late April and early May. In 1987, the average temperature was lower (11.1-13.3°C) during this period, while rainfall was relatively high (125 mm), and aphid reproduction did not begin until the beginning of June (Kuroli et al., 1988).

High rainfall is not favourable to A. craccivora populations since aphids do not survive periods of heavy rain. Severe tornadoes can stop swarms of aphids, while heavy rains can destroy colonies on young plants, where foliage is not plentiful enough to protect them (Mayeux, 1984). Natural enemies can also limit population build up of aphids.

The sowing date of crops influences A. craccivora direct feeding damage. Groundnuts sown early have a better chance of producing a good yield, as they go through a key period of growth before aphid populations build up to high levels. Sowing date was found to be an important factor determining the yield of field beans in the Sudan, with seed yield/plant being positively correlated with number of pods and negatively with percentage infection with Sudanese broad bean mosaic virus (SBBMV), which is transmitted by A. craccivora and Acyrthosiphon sesbaniae (Salih et al., 1973). The close spacing of groundnuts can deter A. craccivora and is also an important cultural factor influencing yield loss (Mayeux, 1984).

Indirect Damage

Honeydew
Indirect damage caused by A. craccivora is due to the production of honeydew and the transmission of plant viruses. Aphid honeydew is a digestive product with a very high sugar content. It builds up on plants when high aphid numbers occur, and acts as a substrate for fungal growth, particularly of sooty moulds. Plant respiration and photosynthetic efficiency are adversely affected (Mayeux, 1984).

Virus transmission
A. craccivora is an important vector of plant viral disease, transmitting over 30 plant viruses, including groundnut rosette, groundnut (peanut) mottle and subterranean clover stunt. It also a vector of a range of viruses of beans, cardamoms, groundnuts, peas, beet, cucurbits and Cruciferae (Blackman and Eastop, 2000). A. craccivora is polyphagous, and reservoirs of aphids and associated disease infection can exist on non-crop plants throughout the year.

Groundnut rosette virus
Groundnut rosette virus (GRV) is a complex of at least five viruses, varying in distribution. GRV is transmitted in a persistent manner by A. craccivora, and may persist in aphids for more than 10 days (Mayeux, 1984). Groundnut rosette can cause serious morphological disturbances to groundnut plants, which take on a bushy appearance. Other symptoms include yellowing, mottling, leaf mosaic, and stunting and distortion of the shoots. It can account for extensive yield losses. If plants are infected when young, they may produce no nuts. The complex of GRV strains, along with an assistor luteovirus (GRAV) and satellite RNAs cause groundnut rosette disease. Distinct disease types have been recognised, dependent on the GRV strains involved: groundnut chlorotic rosette disease, groundnut green rosette disease and groundnut mosaic rosette disease. A. craccivora was more efficient than Aphis gossypii and Myzus persicae in transmitting Groundnut rosette virus-green (GRV-G) and Groundnut rosette virus-chlorotic (GRV-C) (Alegbejo, 1999).

The GRV complex was first described in Africa in 1907, when it strongly affected groundnut production. It has continued to do so, for example, infecting 80-90% of groundnut plants in the Belgian Congo in 1939 (Réal, 1955); and causes high pod yield losses (Bock, 1973; Olorunju et al., 1991). A. craccivora is now considered the most important insect pest of groundnuts in Africa because it transmits GRV persistently (Wightman and Wightman, 1994). Alegbejo and Abo (2002) reviewed the aetiology, ecology, transmission and control of groundnut rosette disease, which appears to be restricted to Africa.

Major yield losses result when secondary spread within the crop occurs due to aphid vectors. GRV can spread rapidly within a groundnut field. In a study in Tanganyika, low infestation of aphids was noted on 16 January, while the first plants with rosette infestation were found on 22 January. A tenfold increase in infestation occurred in the next 2 weeks accompanied by rapidly increasing aphid numbers, with 65% of plants in that field infested with GRV by late February (Evans, 1954).

In a study in Niger in 1981, yields in groundnut crops were 1350 kg/ha following low aphid infestations, compared with 183 kg/ha following high infestations of aphids carrying GRV (Mayeux, 1984). A typical groundnut yield in Africa would be around 450-670 kg/ha, but using insecticides and other management practices yields over 1300 kg/ha can exceptionally be achieved.

Groundnut varieties resistant to GRV were found in Africa in the early 1950s. Systematic plant breeding programmes have been in operation since then (Evans, 1954; Mayeux, 1984). In studies conducted in Nigeria, eight genotypes that were either resistant or susceptible to GRV were planted and infested with viruliferous A. craccivora. Infestation with rosette resulted in a seed yield 33 times higher in the resistant genotypes than in the susceptible ones, while yields were comparable in the two groups under rosette disease-free conditions (Olorunju et al., 1991). It has been reported that GRV resistant varieties from one region in Africa may succumb if grown in another region (Anon., 2000).

Sowing as early as possible in the rainy season, close crop spacing, and the use of insecticides are the recommended methods for controlling GRV in groundnuts in Africa (Farrell, 1976). In Nigeria, for example, dense crops were less heavily colonized than sparse crops (A'Brook, 1964, 1968). In a survey of groundnuts in Malawi, Zambia and Zimbabwe, economic losses due to GRV were low, which was attributed to A. craccivora, the principal vector, being controlled by natural processes, and to the practice of early and synchronous sowing (Wightman and Wightman, 1994).

Insecticides have given yield increases of over 650 kg/ha of shelled groundnuts in rainfed forests and over 1000 kg/ha under irrigation in rosette-prone crops. Insecticide spraying must be done before disease symptoms appear and before aphids can easily be found, however, to give maximum yield advantages; while some farmers may be reluctant to spray seemingly uninfested crops (Anon., 2000).

In India, the incidence of GRV was 4.9% in bunched and 3.3% in spreading varieties of groundnut, while incidence of GRV was nearly twice as high in irrigated compared with rain-fed crops. The loss in yield varied from 27 to 100%. There was a positive correlation between infestation with A. craccivora and the incidence of rosette disease. Close spacing and late weeding were highly effective in reducing aphid infestation and virus infection, and in increasing yield (Kousalya et al., 1971, 1973).

Infections of Groundnut rosette assistor virus (GRAV), in the absence of GRV and its satellite RNAs, reduced leaf area, decreased plant height, reduced the dry weight of haulms and reduced seed weight in four genotypes of groundnut, indicating that infections of GRAV alone can affect plant growth and contribute to yield losses (Naidu and Kimmins, 2007).

Peanut mottle and groundnut stunt viruses

Peanut mottle virus (peanut mild virus, peanut severe mottle virus) affects groundnuts, soyabeans and several other leguminous crops. It causes mottling with necrosis and mosaic symptoms. Leaf crinkling or other malformations can occur, while photosynthetic efficiency is reduced. A. craccivora transmits this virus in a non-persistent manner, and aphids can remain infective for 2 hours (Bock, 1973; Brunt et al., 1996).

In a survey of groundnuts in Hubei, China, it was reported that infestation by groundnut (peanut) mild mottle virus, transmitted by A. craccivora, was between 1 and 98%. In experimental trials, the mild mottle virus reduced groundnut yields by up to 23% (Xu et al., 1983). Infection with Peanut mottle virus led to a mean yield loss of 20%/plant in Georgia, USA, in 1973 (Kuhn and Demski, 1975). Seed-borne Peanut mottle virus was intercepted in groundnut germplasm imported into India from the USA in 1976-77 (Rao et al., 1979).

A. craccivora was found to be an important vector of Peanut stunt virus in lucerne in Sudan. Reservoirs of aphids and virus infection could spread to other leguminous crops, and it has been recommended that lucerne cultivation should not be introduced into the main groundnut-growing areas of the Sudan (Ahmed and El Sadig, 1985).

A. craccivora was reported transmitting five isolates of Peanut stripe virus (PStV) on groundnut in China (Chen et al., 1999).

Other viruses

Subterranean clover stunt virus (SCSV) infects all varieties of Trifolium subterranean, and many species of Medicago and Trifolium. It is spread in a persistent manner by A. craccivora and several other aphids (Brunt et al., 1996). In Australia and New Zealand, A. craccivora is an important pest of pasture grasses, largely because it is a vector of SCSV, which causes mild or severe stunting, marginal chlorosis and puckering of leaflets, and stunting and yellowing of new growth (Gutierrez et al., 1974a, b; Ashby et al., 1982). A. craccivora is also a vector of SCSV in broad bean in Tasmania, where extensive clover plantings potentially act as a reservoir of aphids and virus infection (Johnstone, 1978).

Bean common mosaic virus (BCMV) (bean mosaic virus, bean western mosaic virus, mungbean mosaic virus) infects Phaseolus spp. and a range of other bean and pea crops worldwide. The related Bean yellow mosaic virus (BYMV) also infects Phaseolus and peas, causing necrosis and mottling, although it also causes mottling in groundnuts. A. craccivora transmits BCMV and BYMV in a non-persistent manner (Brunt et al., 1996). For example, A. craccivora transmits both BCMV and BYMV in green beans (Phaseolus vulgaris) in New Zealand (Malone and Hartley, 1978). BCMV was identified occurring on cowpea (Yadav, 2010) and French bean (Phaseolus vulgaris) (Verma and Gupta, 2010) in India, and was transmitted through sap, by seed and by aphids, including A. craccivora.

In the Philippines, mungbeans were most susceptible to mungbean mosaic virus at an early growth stage. A. craccivora was the only insect vector, transmitting the virus in a non-persistent manner even at low aphid densities. The earlier the plant became infected, the higher the percentage of infected seeds (Khan and Lapis, 1989). Mungbean infected in Iran by a virus described as a mungbean strain of Bean common mosaic virus (M-BCMV), which caused deformation, puckering, rolling, blistering and mosaic symptoms, reduced yields by 31-75%, particularly when infection occurred before pod set (Kaiser and Mossahebi, 1974).

A. craccivora was recorded transmitting Soybean mosaic virus (SbMV) in Illinois, USA (Halbert et al., 1981, 1986).

A. craccivora is a significant vector of several viruses of lupins, including BYMV and Cucumber mosaic virus (CMV). In Australia, aphids decrease the grain yield of lupins directly, when large numbers of aphids colonize plants late in the growing season, but mainly cause economic damage via the spread of CMV infection. Incoming viruliferous alatae initiate the infection and yield loss is greatest when aphids arrive early in the crop's development. Intensive insecticide treatments against A. craccivora (and also Myzus persicae), in Australian field experiments, decreased CMV infection, and increased grain yields by up to 35% (Bwye et al., 1997).

In Iran, A. craccivora is an important vector of a number of viruses of leguminous crops, including BYMV, CMV, Alfalfa mosaic virus (AMV), and Pea-leaf roll virus (PLRV) in lentil. In field inoculation studies in lentil with these viruses, yield was reduced by 46-94%. Transmission of CMV and PLRV by A. craccivora in cowpeas and broad beans can also cause yield losses of this order (Kaiser, 1973a, b).

Six aphid species, including A. craccivora, transmitted Bean leafroll virus (BLRV) in a circulative persistent manner on Vicia fabae in Egypt (El-Beshehy and Azza, 2013), and A. craccivora transmitted Cowpea aphid-borne mosaic virus (CABMV) in a non-persistent manner in cowpea in Saudi Arabia (Damiri et al., 2013).

A new virus involved with leaf crinkle disease of urdbean (Vigna mungo) was observed in Himachal Pradesh, India. The virus was transmitted by A. craccivora and via seed and sap (Sharma et al., 2014).

An unknown virus isolated from Senna hirsuta in Nigeria and tentatively designated as Senna mosaic virus (SeMV) was transmitted by A. craccivora in a non-persistent manner (Owolabi and Proll, 2001).

An unknown or uncommon member of the family Luteoviridae causing yellowing and stunting symptoms on chickpea and faba bean was observed in Ethiopia. The name Chickpea chlorotic stunt virus was proposed for this disease. A. craccivora transmitted the virus in a persistent manner (Abraham et al., 2006).

In field studies in Turkey, 10% of aphids of A. craccivora were viruliferous with Plum pox virus-T (Caglayan et al., 2013).

A. craccivora has also been recorded as a vector of Onion yellow dwarf virus (OYDV) (Kumar et al., 2009), Papaya ringspot virus (PRSV) (Kalleshwaraswamy and Kumar, 2008; Kumar et al., 2010; Isha Bhoyer et al., 2014), Pepper veinal mottle virus (PVMV) (Fajinmi et al., 2011), Watermelon mosaic virus (WMV) and Zucchini yellow mosaic virus (ZYMV) (Haque et al., 2004), Sunflower mosaic virus (SMV) (Singh et al., 2005), Faba bean necrotic yellows virus (FBNYV) (Vega-Arreguín et al., 2007) and Faba bean necrotic stunt virus (FBNSV) (Grigoras et al., 2009).

• Pest and disease transmission