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Plantwise Technical Factsheet

wheat aphid (Sitobion avenae)

Host plants / species affected
Avena sativa (oats)
Dactylis glomerata (cocksfoot)
Hordeum distichon (two-rowed barley)
Hordeum vulgare (barley)
Oryza sativa (rice)
Poa annua (annual meadowgrass)
Poaceae (grasses)
Secale cereale (rye)
Triticale
Triticum (wheat)
Triticum aestivum (wheat)
Zea mays (maize)
List of symptoms/signs
Inflorescence  -  discoloration panicle
Leaves  -  abnormal colours
Symptoms

There is no set of clear symptoms for S. avenae infestations on leaves or earheads. Early yellowing of upper leaves and ears could be observed after a heavy infestation but is not specific to S. avenae. The same type of symptoms could also be due to other aphid species or several plant pathogens.

Prevention and control

Cultural Control

In temperate zones early sowing enables aphids to invade early in the autumn, thus enhancing the spread of Barley yellow dwarf virus. Early-sown fields may also have larger overwintering S. avenae populations than late-sown fields, and subsequently earlier and higher aphid populations in spring (Dedryver and Tanguy, 1984). When compatible with other agricultural practices, late sowing in autumn leads to a reduction in S. avenae infestations.

Some practices such as increasing seed rate and undersowing could benefit natural enemies (Powell, 1983). High levels of nitrogen fertilization, often applied in split doses, retard alate formation and increase S. avenae fecundity as the flag leaf remains green during grain-filling.
The use of intercropping as a strategy for increasing the biodiversity of natural enemies in fields has the potential to reduce pest damage and improve the crop production. In a field study in China, intercropping wheat with pea, especially with an 8:2 row pattern of wheat-pea, led to a reduction in the population of S. avenae and improved the stability and sustainability of the aphid’s natural enemies compared with wheat monoculture (Zhou et al., 2009a, 2013). Intercropping wheat with mung bean (Vigna radiata) (Xie et al., 2012) and oil seed rape or garlic (Chi et al., 2014; Nassab et al., 2013) has also been successful in suppressing population growth of S. avenae and increasing the population density of natural enemies of the aphid compared with wheat monoculture. However, intercropping wheat with walnut increased damage caused by S. avenae compared with wheat monoculture (Wang et al., 2014).

It is becoming increasingly important to use mixed wheat cultivars to control wheat pests (Hu et al., 2015). A field study in China indicated that the intercropping of a field cultivar (Beijing 837) with wheat cultivars with different levels of resistance to aphids led to reduced populations of S. avenae and increased populations of its parasitoids (Zhou et al., 2009b).

Host-Plant Resistance

Different levels of infestation by S. avenae among wheat varieties have been observed by many authors: in England (Lowe, 1984), the Czech Republic (Havlickova, 1990, 1993), Pakistan (Hamid, 1988; Karimullah and Ahmad, 1989), the former USSR (Krivchenko and Radchenko, 1988; Radchenko, 1989), China (Zhang et al., 1989) and France (Dedryver and di Piétro, 1986; Piétro and Dedryver, 1986; Piétro et al., 1998). Wheat varieties C273 from India and Lanmai from Shaanxi, China, have shown high levels of resistance in field experiments in China (Liu et al., 2006, 2014). Resistance has been attributed to non-preference, but mainly antibiosis, mechanisms (e.g. Chen et al., 1997; Niraz et al., 1996; Silva et al., 2013). However, the impact of infestation on yield is not obvious and no strong resistance genes were found in hexaploid commercial varieties. Most differences in population levels could be due to differences in precocity, to some morphological differences (e.g. awned ears are less favourable to S. avenae than awnless ones) and to differences in hydroxamic acid content (mainly at young stages of the plants) (Nicol et al., 1993). More promising would be to introduce in hexaploid wheats stronger antibiotic resistance found in other Triticineae, e.g. in Triticum monococcum (Sotherton and Van Emden, 1982; Caillaud et al., 1994). A study by Guan et al. (2015) indicated that the resistant diploid line ACC20 PGR1755 may provide a valuable resource in breeding wheat for resistance to S. avenae. Transgenic lines, for example, containing the snowdrop lectin gene, may play a role in conferring resistance to S. avenae in the future (Stoger et al., 1999; Miao et al., 2011; Nakasu et al., 2014).

Chemical Control

For autumn barley and wheat, chemical control has to be applied during the period of overlap between aphid flight and seedling emergence and repeated immediately afterwards. In spring it is usually done on wheat between ear emergence and flowering; delayed sprays are ineffective or uneconomical. Many insecticides are effective on aphids, for example, carbamates and pyrethroids (Wiles and Jepson, 1992), but most of them are also harmful to parasitoids and predators. Seed treatments with systemic insecticides (e.g. imidacloprid) are efficient to prevent autumn infestations and consequently BYDV spread (Knaust and Poehling, 1992) because of their prolonged persistence in the plants. Their long-term consequences on the aphid and its natural enemy populations are not known. S. avenae is reported to have developed resistance to several commonly used insecticides in China (Chen et al., 2007) and has recently developed resistance to pyrethroids in the UK, resulting in control failure at some locations in England in 2011 and 2012 and associated local epidemics of BYDV in 2012 (Foster et al., 2012; Dewar et al., 2014).

At flowering time, farmers often mix an aphicide with a fungicide that has to be applied at the same time. This fungicide could affect the development of Entomophthorales in areas where they control aphid populations, but this point remains unclear.

S. avenae is not regularly sprayed during spring or summer on other cereals than wheat.

Semiochemicals may have potential in the control of S. avenae. In laboratory and field experiments, settlement of S. avenae was significantly reduced on wheat seedlings treated with either Tasmannia stipitata plant extract (which contains the antifeedant polygodial) or cis-jasmone (a stress related volatile plant activator inducing defence mechanisms within the wheat plant), and in semi-field trials parasitism of S. avenae by the parasitoid Aphidius ervi was significantly higher on plants baited with nepetalactone (an aphid sex pheromone component attractive to aphid parasitoids) compared with untreated controls (Bruce et al., 2002, 2003). A field study in China compared the use of intercropping (wheat with oilseed rape) with and without the application of semiochemicals (methyl salicylate, MeSA) to alter local arthropod populations in an effort to improve control of S. avenae on wheat. Aphid densities were lowest and grain yield and quality were highest when intercropping and MeSA release were combined, emphasizing the need to integrate alternative pest control approaches to optimize sustainable insect pest management (Wang et al., 2011).

Pest Forecasting

Many attempts have been made, mainly in Europe, to forecast S. avenae outbreaks or damage, with the help of mathematical models: e.g. in the Netherlands (Carter et al., 1982), the UK (Entwistle and Dixon, 1986; Mann et al., 1986), Germany (Rossberg et al., 1986) and France (Pierre and Dedryver, 1984, 1985; Plantegenest, 1995). All of them are useful tools for scientific purposes, but their practical use by farmers’ needs aphid counts in the field, which reduces their attractiveness.

Models have been constructed using degree-days to determine the timing of spring migration of holocyclic populations of S. avenae and Rhopalosiphum padi from winter hosts (Hansen, 2006) and for predicting the increase of S. avenae in wheat (Richter, 2010). Such models can be used as part of a decision support system for the chemical control of cereal aphids.

A preliminary spatially explicit model was developed to forecast aphid population dynamics (using S. avenae as the target species) at the scale of a whole country (metropolitan France). It is hoped that after suitable validation over several years this model will be used to forecast aphid densities and yield losses and lead to a decrease in insecticide sprayings in wheat crops (Ciss et al., 2014).

A simulation model (GETLAUS01), which has been developed to simulate the population dynamics of cereal aphids (S. avenae, Rhopalosiphum padi and Metopolophium dirhodum) in the presence of natural enemies on wheat (Gosselke et al., 2001; Freier et al., 2002), was tested along with two other simulation models (SIMLAUS and LAUS) to determine cereal aphid populations in Germany over several years. Simulation runs with the model SIMLAUS accurately predicted (in 96% of case studies) the type of hibernation of S. avenae and R. padi in fields of both winter wheat and winter barley, but the model was not suitable for predicting the number of aphids found in cereal crops in the autumn. In 12 of 35 case studies, the model LAUS predicted accurately, from a priori data, the populations of S. avenae in cereal fields during spring and early summer. The model GETLAUS01 produced close relationships between the observed and predicted populations of cereal aphids found during the summer in crops of winter wheat. The possibility of using revised versions of these models as an integral part of pest management is discussed (Klueken et al., 2009).

Botanicals

The effect of natural insecticides (e.g. from Azadirachta indica and Quassia amara) on S. avenae has been investigated by Sengonca and Brüggen (1991), West et al. (1992), Holaschke et al. (2006) and Bushra et al. (2014).

Laboratory and field studies in Pakistan showed that the cost-benefit ratio of using neem (Azadirachta indica) seed kernel extract against S. avenae on wheat was comparable to that of imidacloprid and it may be considered as a promising substitute of synthetic insecticides to control wheat aphids (Aziz et al., 2013).

Biological Control

During the 1960s the cereal aphids, S. avenae and Metopolophium dirhodum become a serious problem for wheat growers in Chile, necessitating the application of insecticides over 120, 000 ha to prevent losses amounting to some 20% of the crop from the feeding of the aphids and from barley yellow dwarf luteovirus which they transmit. An IPM programme was initiated in 1975, which included the breeding and release of nine species of parasitoids and five coccinellid predators imported from Europe, Israel, North America and South Africa. Four of the parasitoids and one predator, Hippodamia variegata, became established. Satisfactory control of both aphids was obtained. Three of the parasitoids - Aphidius uzbekistanicus, A. rhopalosiphi and Praon volucre - aided by native predators, maintain control of S. avenae (Zúñiga et al., 1986). In 1978, cultures of the natural enemies were sent to Brazil and in 1981 were sent from there to Argentina (Altieri and Klein-Koch, 1989). Similarly satisfactory results have been obtained in both these countries.

The efficiency of the predator Harmonia axyridis feeding on cereal aphids (Rhopalosiphum padi and S. avenae) was found to be affected by nitrogen availability. In no-choice feeding trials, H. axyridis consumed more aphids on plants receiving low levels of nitrogen, probably because the aphids were smaller than on plants receiving higher levels of nitrogen. An understanding of the predator-prey interactions could help improve the biological control of cereal aphids at any particular level of nitrogen fertilizer treatment in the field (Aqueel and Leather, 2012).

Sprays of the entomopathogenic fungi Verticillium lecanii are effective in reducing the numbers of S. avenae and could be used as a complementary strategy in integrated pest management programmes against cereal aphids, although the entomopathogenic fungi may reduce the efficiency of other biocontrol agents (parasitoids and predators) when applied simultaneously (Aqueel and Leather, 2013).

 

Impact

Introduction

S. avenae is found on numerous species of Poaceae worldwide, and is a pest of cereal crops in temperate regions. It is a major pest of wheat (Triticum aestivum) in Europe (Carter et al., 1980), North America (Foott et al., 1979; Feng et al., 1993a, b), South America (Lopez et al., 1986; Quiroz et al., 1986), Central Asia (Sokolov, 1980; Udachin et al., 1984) and China (Liu et al., 1986). It is considered a secondary pest on rice (Oryza sativa), maize (Zea mays), barley (Hordeum vulgare), and certain other cereals (Kieckhefer et al., 1980; Osler, 1981; Hinz, 1985; Coderre and Tourneur, 1988; Coceano and Peressini, 1989; Pons et al., 1989a, b).

S. avenae causes direct damage by feeding on fruits, leaves, stalks and ears, and indirect damage by excreting honeydew and transmitting viruses. S. avenae mainly impacts cereal yields by removing plant nutrients and reducing photosynthesis via honeydew accumulations.

Direct Feeding Damage

S. avenae outbreaks can be very damaging to cereal yields, especially in wheat. Damage due to S. avenae manifests itself as reduced number of heads, reduced number of grains per head, and reduced grain or seed weight (usually expressed as 1000-grain weight) (Rautapää, 1966; Kolbe and Linke, 1974; Hinz and Daebeler, 1976a).

Wheat yields can be reduced by around 20-30% during outbreaks (Kolbe and Linke, 1974). Yield reductions of 11.5-43.4% were reported in a 3-year German field study, on a range of different wheat cultivars. The average grain weight/ear and 1000-grain weight were reduced in all cultivars by S. avenae infestation, although some degree of tolerance was reported (Hinz and Daebeler, 1976a). Yield reductions in these experiments were highest when heavy infestations occurred early in plant development (Hinz and Daebeler, 1976b). In a field study in the Irish Republic, the estimated yield reductions in untreated April-sown barley due to feeding damage by S. avenae were 0.71 t/ha and 0.83 t/ha (10.6 and 11.3%) in 1996 and 2001, respectively, the two seasons in which this aphid was abundant (Kennedy and Connery, 2005).

S. avenae causes maximum yield loss on wheat between ear emergence and flowering. In a field study in China, for example, wheat yield reductions of up to 14% were observed as a result of early infestation at ear emergence, while yield reductions decreased with later infestations (Liu et al., 1986). In laboratory studies in the USA with spring wheat, feeding by S. avenae caused significant yield losses when plants were infested at the boot stage, but not at the later anthesis and dough stages. Reduced numbers of spikelets/head and reduced average grain weight were the principal components of yield loss (Voss et al., 1997). In a Brazilian greenhouse study, plants infested with S. avenae at the 'stem extension' stage showed a reduction of 38% in the number of grains/ear as compared with uninfested plants, a reduction of 32-37% in grain weight, and a reduction of 50-60% in ear production; seed vigour was also reduced (Butignol and Corseuil, 1982).

Infestations occurring later (during grain ripening) generally do not cause significant yield losses, but can reduce the quality of the flour for breadmaking (Wratten et al., 1979). In cage experiments in the UK, infestations of S. avenae reduced the percentage of flour extracted, while there was an increase in colour, and the nicotinic acid and thiamin (vitamin B1) content of the flour, accompanied by a reduction in baking value and in the glutenin content (Lee et al., 1981). Analaysis of flour from wheat grains naturally infected with cereal aphids in Hungary revealed that aphid infection caused a decrease in the gliadin/glutenin ratio of the wheat, decreasing the bread making quality of the wheat flour. The most significant decrease in gliadin/glutenin ratio was caused by Diuraphis noxia infection, followed by Rhopalosiphum padi and then S. avenae (Basky and Fónagy, 2003). In cage studies using hard-kernel wheat, it was shown that the major factor in yield loss caused by feeding by S. avenae and D. noxia was individual kernel mass reduction and that aphid feeding did not change the protein structure of the hard-kernel wheat (Basky and Fónagy, 2007).

Cereal aphid infestations, and subsequent yield loss, can be dramatically reduced using resistant cultivars. S. avenae infestations on five cultivars of wheat in field cages in Turkey, for example, caused significantly different yield losses, in terms of 1000-grain weight, ranging from 5 to 16.61% (Elmali and Toros, 1997). Winter wheat cultivars grown in studies in Poland and the Czech Republic also differed in their tolerance to S. avenae (Ciepiela, 1993; Havlickova, 1997).

When artificial infestations were used to assess the damage potential of S. avenae and Metopolophium dirhodum in winter wheat in Germany, S. avenae was found to cause significantly higher reductions in dry mass and 1000-grain weight than M. dirhodum on the flagleaf (Niehoff and Staeblein, 1998). In the Netherlands, total yield losses of up to 700 kg/ha on wheat were reported, 72% of which was attributed to direct sucking damage, by the aphids S. avenae and M. dirhodum, and indirect effects of the honeydew they produce (Rabbinge et al., 1981). S. avenae is the dominant cereal aphid species in many European countries, including Slovenia, where it caused direct crop yield reductions ranging from 10 to 50%, and indirect losses of 20 to 80%. The most important factors contributing toward an increase in populations of S. avenae, in this Slovenian survey, were weather conditions, agrotechnical measures (size of parcel, rotation of crops, nutrition, sowing and soil cultivation), presence/absence of natural enemies and the introduction of new cultivars (Trdan and Milevoj, 1999).

Several attempts at defining threshold numbers of S. avenae have been made, with some success; although thresholds have varied and the concept of threshold number has been brought into question (Vereijken, 1979). In the UK, one aphicide spray at the time of flowering has been recommended in wheat if aphid numbers rise above 5 per ear (George, 1974). This scheme, in commercially-grown wheat in the UK, gave an increase in grain yield of about 12.5%. Much lower yield increases were recorded when sprays were applied at a later growth stage or when the number of aphids did not reach the specified level of 5 per ear (George and Gair, 1979). Aphicide sprays applied against S. avenae and M. dirhodum during the booting stage increased average yields by 0.26 t/ha. In another study, grain quality was affected only by high aphid infestations which also caused large yield reductions (Oakley and Walters, 1994). Large-scale field trials on winter wheat in Germany in 1986 showed that an extra yield of 4.0-8.4% could be achieved if chemical control measures against S. avenae were undertaken when infestation was 12-15 aphids/ear. The cost-covering yield from spraying with insecticide averaged 0.14 t/ha, with control being economically justified at infestation levels above 3-5 aphids/ear at the time of flowering (Assmann et al., 1988). The 1000-grain weight was reduced on wheat plants with 4 or more aphids per ear in an Argentinean study (Rios and Conde, 1986). In Idaho, USA, economic thresholds were calculated to be 2-4 aphids/tiller at flowering, 6-10 aphids/tiller up to the milky ripe stage and 10 or more aphids/tiller from the milky ripe to medium-dough stage. Yield increases of 2.7 t/ha (36.5%) and 1.2 t/ha (29.3%) were obtained when sprays were applied at flowering in the two years of this study (Johnston and Bishop, 1987).

The effect of S. avenae damage on yield therefore depends on the size and duration of infestation, the phenological stage of the crop when infested, pesticide applications, cultural practices, use of resistant cultivars, natural enemy abundance, weather conditions, and on other factors, such as foliar disease and dryness, that are liable to increase with aphid damage. In winter wheat, for example, a significantly higher percentage of yield reduction for a given aphid density was obtained when plants were grown under severe water stress versus nonstress conditions (Fereres et al., 1998). A number of simulation models for S. avenae damage on wheat have been developed, to estimate potential yield loss, impose thresholds, and optimize insecticide treatments (Carter et al., 1989; Rossing 1991a, b; Li et al., 1994; Plantegenest et al., 1997).

A crop loss model for S. avenae on high-yielding varieties of winter wheat in southern Sweden was developed based on average annual yield loss in field experiments in 1995-2002. The economic injury level was found to be 7 aphids/tiller with a control cost of 300 SEK/ha and wheat price of 1 SEK/kg. Volume weight and grain weight were only slightly affected by high aphid populations and the protein percentage was unaffected. The economic threshold for high-yielding wheat was calculated as 1 aphid/tiller at crop stage 59, 4 at crop stage 69, and 7 at crop stage 75. These economic injury levels and economic thresholds are important components of a cost-effective integrated pest management programme and are useful for decision making in the application of pesticides (Larsson, 2005). Yield losses of wheat due to S. avenae, Sitobion miscanthi, Rhopalosiphum maidis and Rhopalosiphum padi under field conditions in India ranged from 6.1 to 27.8% when the aphid population level exceeded 50 aphids per ear, and timely-sown wheat suffered more loss (10.7-27.8%) than late-sown wheat (0.4-12.4%) (Paramjit Singh et al., 2008).

Damage on barley, rice, maize, and other cereals, has not been extensively studied. Yield loss on barley due to S. avenae, in one study, was manifested as a reduction in 1000-grain weight. The brewing quality of infested barley was no different to uninfested barley, however, although total b-amylase was reduced in the grain and a-amylase was increased in the malt from infested barley (Rautapää, 1968). Yield losses in spring barley due to feeding by four cereal aphid species were measured in caged plots, artificially colonized with aphids, in South Dakota, USA. Yield losses were greatest when aphids fed during the seedling (2-3-leaf) stage, when mean densities of 25-30 aphids/stem resulted in losses of 50% in some components of yield. However, Schizaphis graminum and R. padi were more damaging than S. avenae at similar population densities on barley (Kieckhefer and Kantack, 1986). In greenhouse studies in the USA, with S. avenae on oats (Avena sativa) infested at the one-leaf growth stage, mean root and shoot dry weights were reduced to 79 and 88% of the control. Spikelets per plant was the yield component most affected by aphid feeding (Gellner and Kieckhefer, 1992).

In host-transfer experiments, wheat clones of S. avenae had lower nymphal developmental times and age at first reproduction when transferred to barley, while barley clones had a lower reproductive period and adult lifespan when transferred to wheat. The results suggested that the wheat clones are more specialized to their host plant, while the barley clones appear to be generalized. The implications of these results for management of the aphid by planting barley in fields adjacent to those of wheat and intercropping wheat with barley are discussed (Gao and Liu, 2013). A further study showed that barley clones of S. avenae had significantly lower fecundity and tended to have longer developmental times when transferred to oat. However, oat clones developed faster after they were transferred to barley. These results indicate that the barley clones are specialized to a certain extent, while the oat clones appear to be generalized (Gao et al., 2014).

Honeydew and Fungal Pathogens

Honeydew, a sugar-rich aphid secretion, can cause physiological changes and chlorotic symptoms in leaves, and affects net carbon dioxide assimilation in wheat (Rossing and van de Wiel, 1990; Rossing, 1991a). Honeydew probably also causes an early senescence of leaves (Vereijken, 1979). Honeydew from S. avenae appears to be particularly disruptive to photosynthesis of cereals in laboratory and field studies (Rabbinge et al., 1981). Yield losses due to honeydew, as a result of high infestations early in the season, can be considerable; although simulations show that later in the growing season damage caused by honeydew decreased whilst that caused by aphid feeding remained constant (Rossing, 1991b). In simulation models based on actual yield reductions in the Netherlands (around 13%), honeydew was responsible for the major part of the damage (Van Roermond et al., 1986). Honeydew production and its effect in encouraging the growth of secondary fungal pathogens may account for more than 60% of total yield loss (Rabbinge and Vereyken, 1980). The effects of combined attack of wheat by S. avenae and the fungal pathogens Septoria nodorum (wheat glume blotch) and Puccinia recondita (brown rust) have been studied in Germany (Brink and Drews, 1994; Drews, 1995).

Indirect Damage by Virus Transmission

S. avenae is an important vector of Barley yellow dwarf virus (BYDV), which it transmits in a persistent manner. S. avenae is a major pest of barley, and a secondary pest of wheat, in its role as a vector of BYDV. This virus has been extensively studied in western Europe and northern America (Plumb, 1983). Of the six strains within the BYDV complex, S. avenae is a major vector of two: BYDV-MAV and BYDV-PAV (Brunt et al., 1996). Depending on region, S. avenae could be the main vector for primary infection of cereals with BYDV in autumn (the UK), or involved in virus dissemination in the spring within barley, wheat or maize crops (Leclerq et al., 1995).

In a study in winter wheat in Virginia, USA, autumn infection with BYDV (predominantly BYDV-PAV), significantly reduced grain number, grains per head, and 1000-grain weight, by 28, 22, and 34%, respectively (Herbert et al., 1999). Average yield losses in wheat due to BYDV in Santiago, Chile, over a 9-year period were around 10%, with S. avenae being one of the main virus vectors (Herrera and Quiroz, 1988). In the Netherlands, aphids (S. avenae and Rhopalosiphum padi) were controlled in winter wheat to prevent serious crop damage by BYDV. Large numbers were present on wheat that already showed BYDV symptoms at the time of treatment, while control resulted in a yield increase of approximately 2 t/ha (Timmer, 1996). Reductions in wheat yields due to BYDV were estimated in a severe outbreak year in Germany to be up to 40%, with the epidemic mainly caused by an early spring immigration of S. avenae (Borgemeister and Poehling, 1991). In a Yugoslavian study, the incidence of BYDV in maize exceeded 80%, and yield losses were 50-75%; with S. avenae being one of the two vectors recorded (Balaz and Tosic, 1992). Laboratory studies have shown that barley infected with BYDV is a more favourable host plant than uninfected barley for both the brown and green colour morphs of S. avenae, particularly the green colour morph (Hu et al., 2014).

S. avenae is a minor vector of Maize dwarf mosaic virus, mainly within maize, Bean yellow mosaic virus and Pea mosaic virus, all transmitted in a non-persistent manner; and Beet western yellows virus (as radish yellows virus), which is transmitted in a persistent manner (Brunt et al., 1996; Blackman and Eastop, 2000). S. avenae is also a vector of the causal agent of rice giallume, a virus closely resembling BYDV and an important disease of rice in Italy, where it sometimes causes yield losses of almost 100% (Osler, 1981; Osler et al., 1984). S. avenae successfully transmitted Sugarcane mosaic virus under glasshouse conditions (Tahira Yasmin et al., 2011).

Related treatment support
Plantwise Factsheets for Farmers
Zhang, Y.; CABI, 2014, Chinese language
Hasnain, M.; CABI, 2012, English language
Hasnain, M.; CABI, 2012, Urdu language
 
Pest Management Decision Guides
Han, Z. L.; CABI, 2015, English language
Sileshi, F.; CABI, 2015, English language
Michael, D. W.; Tsegay, M.; Lemma, H.; CABI, 2014, English language
 
External factsheets
Plant Health Australia Factsheets, Plant Health Australia, English language
DPI NSW factsheets, New South Wales Government, Department of Primary Industries, Australia, 2011, English language
USDA-NAL National Invasive Species Information Center Species Profiles, USDA-NAL National Invasive Species Information Center (NISIC), 2012, English language
Bayer CropScience Crop Compendium, Bayer CropScience, English language
PlantVillage disease guide, PlantVillage, English language
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