EPPO Global Database

Cyst nematodes of maize: addition of Heterodera zeae and Punctodera chalcoensis to the EPPO Alert List

In their recent review, Nicol et al. (2011) focus on nematode species that may present a threat to agriculture worldwide. Considering maize (Zea mays) cultivation, they explain that more than 60 nematode species have been found associated with maize in different parts of the world. Most of these species have been recorded from roots or soil around maize roots but for many of them data is lacking on their biology and pathogenicity. The most important groups of plant parasitic nematodes which are limiting factors in maize production include root knot nematodes (Meloidogyne spp.), root lesion nematodes (Pratylenchus spp.) and cyst nematodes (Heterodera spp.). Among cyst nematodes, more than 9 species have been recorded as being associated with maize in subtropical and tropical countries, but only three (Heterodera avenae, Punctodera chalcoensis and H. zeae) are considered economically important.

H. avenae is a cosmopolitan species (also widespread in the EPPO region) and a well-known pest of cereals (wheat, barley, oat, rye). Although there is limited information on its pathogenicity on maize, the fact that it can be associated with this crop could be important in wheat/maize production systems.
Punctodera chalcoensis has only been reported from Mexico where it causes significant economic damage to maize crops. Its host range is limited to maize and teosinte (Euchlaena mexicana).
H. zeae was first described in 1970 from a village in India (Chapli, Udaipur district, Rajasthan), and it is now known to be widely distributed in the major maize-growing areas of northern, central, eastern and western parts of India. In Asia, this nematode has been reported from Nepal, Pakistan and Thailand. H. zeae is also known to occur in the Nile valley in Egypt. In the USA, H. zeae was first recorded in Maryland (in 1984) and then in Virginia (in 1992). In the USA, it is considered as an exotic and introduced species, and phytosanitary measures were put in place when it was discovered. However, in 1996, the US federal regulations for H. zeae were lifted on the basis that the infestation was contained by the two states affected. In Europe, H. zeae was reported for the first time in Portugal in 2002. During a survey on Heterodera species, cysts and second-stage juveniles (J2) of H. zeae were recovered from soil samples collected near a fig tree (Ficus carica) and from two maize fields in three different localities in the Central region: Pego (municipality of Abrantes), São Facundo (municipality of Abrantes) and Granja (municipality of Coimbra).

Considering the importance of maize cultivation in the EPPO region, the EPPO Panel on Diagnostics in Nematology suggested that Heterodera zeae and Punctodera chalcoensis should be added to the EPPO Alert List.

Punctodera chalcoensis (Nematoda: Heteroderidae) – Mexican corn cyst nematode

Why: Punctodera chalcoensis is a cyst nematode which causes economic damage to maize crops in Mexico. Damage observed in the maize-growing area of Huamantla (Tlaxcala state) was first attributed to a Mexican race of Heterodera punctata. In 1976, it was found that the Mexican specimens differed from P. punctata and belonged to a distinct species which was called Punctodera chalcoensis (type specimens were collected near Chalco, state of Mexico). Considering the importance of maize cultivation in the EPPO region, the EPPO Panel on Diagnostics in Nematology suggested adding P. chalcoensis to the EPPO Alert List.

Where: P. chalcoensis is widespread in Mexico in temperate maize-growing areas. Its presence has been reported at least in the following states: Jalisco, México, Michoacán, Puebla, Querétaro, Tlaxcala, Veracruz. Considering the very limited world distribution of P. chalcoensis and the fact that it feeds only on maize and teosinte (a close relative), it is suggested that P. chalcoensis is indigenous to Central Mexico and that it has co-evolved there with maize.

North America: Mexico (Jalisco, México, Michoacán, Puebla, Querétaro, Tlaxcala, Veracruz).

EPPO region: absent.

On which plants: The host range of P. chalcoensis is limited to maize (Zea mays) and teosinte (Euchlaena mexicana).

Damage: Infested maize fields show patches of stunted and chlorotic plants. In heavily infested sandy soils, plants are markedly stunted with chlorotic leaves exhibiting pale colour stripes. The root system of attacked plants is generally poorly developed. Two months after planting (at the beginning of the rainy season in Mexico), large numbers of white females can be observed on the root surface of infested plants. Damage is more severe during the rainy season, as precipitation stimulates the emergence of juveniles and subsequently favours the invasion of the roots. P. chalcoensis survives and reproduces well in all soil types, but damage is more severe on volcanic sandy soils. Attacked roots are also prone to secondary infections by other pathogens. Studies carried out in the 1980s showed that under glasshouse conditions, a yield reduction of about 60% could be obtained with maize plants grown in heavily infested soils. Under certain conditions, especially when pathogenic fungi are present, it has been reported that P. chalcoensis could significantly reduce maize yield (up to 90%). Although yield losses in maize fields infested by P. chalcoensis are considered to be high in Mexico, information on economic losses is generally lacking.

P. chalcoensis is a sedentary endoparasitic nematode. It has one generation per year and survives winter in diapause. A period of hibernation is required to break diapause and stimulate the emergence of second-stage juveniles in the following spring. Under experimental conditions, the life cycle is completed in approximately 30 to 50 days. The males mature earlier than the females, emerge from the host root, then move towards the females and mate with them. Eggs are produced after fertilization and are retained in the female body. Females form spherical cysts, pale to dark brown, darkening with age which may contain 200 to 400 eggs. Second-stage juveniles emerge from the cysts, penetrate host roots and establish a specialized feeding site (syncytium) in root tissues.

Dissemination: As with most cyst nematodes, dissemination is largely ensured by passive transport with soil, water, and plant material. The mobile stages (juveniles, males) can only move over very short distances. There is no data on the longevity of cysts in the soil, but as for other cyst nematode species it is likely that P. chalcoensis cysts remain viable in the soil for several years.

Pathway: Infested soil and growing media, plants for planting, bulbs and tubers from areas where P. chalcoensis occurs are the most probable pathways to introduce this pest into the EPPO region. Soil attached to machinery, tools, footwear, or plant products is also another possible pathway.

Possible risks: Maize is widely grown in the EPPO region and is of major economic importance. Cyst nematodes generally are difficult to control once established because of the persistence of the cysts in the soil. In Mexico, differences have been observed in maize susceptibility but no resistant cultivars have been identified. There is no data on the impact of crop rotation to diminish the nematode populations, although it is likely to be effective. Other cultural methods, such as early sowing (before hatching of juveniles) and good plant nutrition are likely to reduce the impact of the pest. Nematicide treatments are becoming more and more difficult to apply in field crops for economic and environmental reasons. Although more data is needed on the economic impact of P. chalcoensis on maize, it is generally reported from Mexico that it can reduce maize yield and cause economic losses. As it has been observed in temperate areas of Mexico (e.g. in regions above 2000 m altitude), it seems likely that this species has the potential to establish in the EPPO region, although more data on its biology would be needed to verify this assumption.

Heterodera zeae (Nematoda: Heteroderidae) –Corn cyst nematode

Why: Heterodera zeae is a cyst nematode which has been reported from different parts of the world on maize and other Poaceae. H. zeae was first described in India where it is considered to be the most important nematode problem in maize. It is also considered as widespread in Pakistan. Considering the importance of maize cultivation in the EPPO region, the EPPO Panel on Diagnostics in Nematology suggested adding H. zeae to the EPPO Alert List.

Where: H. zeae was first described in 1970 in India where it is now considered as widespread. It was then reported in Pakistan (1980), Egypt (1981), USA (1981), Thailand (1995), Nepal (2001), and Portugal (2002).

Africa: Egypt.

Asia: India (Andhra Pradesh, Bihar, Chhattisgarh, Delhi, Gujarat, Haryana, Himachal Pradesh, Jammu and Kashmir, Jharkand, Madhya Pradesh, Maharashtra, Punjab, Rajasthan, Tamil Nadu, Uttar Pradesh, Uttaranchal, West Bengal), Nepal, Pakistan, Thailand.

North America: USA (Maryland, Virginia). H. zeae is considered as an exotic and introduced species (federal regulations were put in place but lifted in 1996, as it was considered that the infestation was contained).

EPPO region: Egypt, Portugal (Central region). H. zeae was detected in 2002 in soil samples collected near a fig tree (Ficus carica) and from two maize fields in 3 localities: Pego, São Facundo (both in municipality of Abrantes) and Granja (municipality of Coimbra). However, since this first record no further information could be found about the current distribution and impact of H. zeae in Portugal.

On which plants: Zea mays (maize) is the major host plant of H. zeae. Other cultivated or wild Poaceae species are also considered as suitable host plants, such as Alopecurus pratensis, Avena sativa (oat), Coix lacryma-jobi, Euchlaena mexicana (teosinte), Hordeum vulgare (barley), Panicum miliaceum (millet), Setaria italica (Italian millet), Triticum aestivum (wheat), Oryza sativa (rice), Saccharum officinale (sugarcane) Sorghum sudanense (Sudan grass), Sorghum vulgare (sorghum), Vetiveria zizanioides (vetiver). Studies conducted in Pakistan on H. zeae populations associated with maize and vetiver have suggested the existence of host races in H. zeae.

In many papers, it is considered that the host range of H. zeae is limited to Poaceae. However, in Pakistan the presence of H. zeae has also been reported on plants of economic importance which belong to other plant families as: Capsicum annuum (sweet pepper – Solanaceae), Citrus (Rutaceae), Corchorus capsularis (jute - Malvaceae), Pyrus communis (pear - Rosaceae), Prunus dulcis (almond - Rosaceae), Raphanus sativus (small radish - Brassicaceae), Solanum lycopersicon (tomato - Solanaceae). More data would be needed to better understand the role of these plant species in the biology of H. zeae and assess the economic impact of the nematode on these crops.

Damage: H. zeae is a sedentary semi-endoparasite which feeds on roots. Affected plants are stunted, pale in colour, with narrow leaves. In the field, stunting frequently occurs in irregular patches. The development of maize tassels may be noticeably delayed and the maize plants bear smaller cobs with relatively fewer grains. The root system is poorly developed with a bushy appearance, and the presence of cysts on the root surface can be observed. In Pakistan, plants of tomato and almond infested by H. zeae were severely stunted. Data on economic losses is generally lacking from countries where the pest occur, however, it has been observed that small numbers of nematodes could cause serious damage (e.g. 29% crop loss at 6 second stage juveniles/cm³ soil in Rajasthan). During microplot experiments conducted in Maryland, it was observed that maize growth and yield could be reduced by 13 to 73% in the presence of H. zeae, and that damage was more severe in coarse-textured soil, as well as under hot and dry conditions.

Temperature plays an important role in the biology of H. zeae, and favourable soil temperatures for most phases of the life cycle lay above 25°C. At temperatures of 10-15°C, only 10-20% of the juveniles emerge from cysts. The total life cycle from egg to reproducing adult is short and takes 15 to 17 days under favourable temperatures (about 27-39°C). It is estimated that under these optimal conditions, H. zeae may complete 6-7 generations during a maize growing season.

Males of H. zeae are rare and reproduction is mainly parthenogenetic. Adult females are pear or lemon-shaped and pearly-white, turning light to dark brown as the cyst matures. Female produces a gelatinous egg mass; a portion of the eggs are deposited in an egg mass surrounded by this matrix. The remainder of the eggs are retained in the female body, which becomes a protective cyst after death.

Dissemination: As with most cyst nematodes, dissemination is largely ensured by passive transport with soil, water, and plant material. The mobile stages (juveniles, males) can only move over very short distances. As for other cyst nematode species, it is likely that H. zeae cysts remain viable in the soil for long periods. During fields and laboratory experiments conducted in Maryland, it was observed that infective H. zeae could survive at least 19 months in a fallow field with fine silty-clay soil and more than twice as long in the laboratory (i.e. up to 51 months at 2°C and 24°C, under moist conditions).

Pathway: Infested soil and growing media, plants for planting, bulbs and tubers from areas where H. zeae occurs are the most probable pathways to introduce or spread this pest into the EPPO region. Soil attached to machinery, tools, footwear, or plant products is also another possible pathway.

Possible risks: Maize is widely grown in the EPPO region and is of major economic importance. Other cereal hosts, such as wheat and barley are also major crops in the EPPO region. Cyst nematodes are generally difficult to control once established because of the persistence of the cysts in the soil. Nematicide treatments are becoming more and more difficult to apply in field crops for economic and environmental reasons. Fields studies conducted in Egypt have showed that crop rotation with non-host plants (Vicia faba and Trifolium alexandrinum) could reduce the nematode populations and prevent damage to the succeeding maize crop. In contrast, when maize was rotated with barley or wheat, nematode populations increased significantly. Concerning the use of resistant cultivars, although few moderately resistant maize cultivars have been identified, almost all tested cultivars have been found to be suitable hosts for H. zeae. Biological control has not been attempted against H. zeae, although some soil-inhabiting fungi (e.g. Arthrobotrys, Dactylaria, Curvularia, Paecilomyces) and bacteria (e.g. Bacillus, Pseudomonas) have showed some effects against H. zeae. Although more data is needed on the current distribution of this nematode in the EPPO region and its impact on maize and other cereal crops, it seems desirable to prevent its introduction or further spread.

EPPO RS 2012/006
Panel review date: -	Entry date 2012-01

Sources

Heterodera chalcoensis

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Hetedodera zeae

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