Invasive Species Compendium

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Datasheet

Globodera tabacum
(tobacco cyst nematode)

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Datasheet

Globodera tabacum (tobacco cyst nematode)

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Globodera tabacum
  • Preferred Common Name
  • tobacco cyst nematode
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Nematoda
  •       Class: Secernentea
  •         Order: Tylenchida

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Pictures

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PictureTitleCaptionCopyright
Globodera tabacum solonacearum infested flue-cured tobacco in the field  showing damage caused by tobacco cyst nematode.
TitleDamage symptoms on tobacco in the field
CaptionGlobodera tabacum solonacearum infested flue-cured tobacco in the field showing damage caused by tobacco cyst nematode.
CopyrightJanet A. Rowe
Globodera tabacum solonacearum infested flue-cured tobacco in the field  showing damage caused by tobacco cyst nematode.
Damage symptoms on tobacco in the fieldGlobodera tabacum solonacearum infested flue-cured tobacco in the field showing damage caused by tobacco cyst nematode.Janet A. Rowe
A scanning electron micrograph of G. tabacum perineum, showing parallel cuticular ridges between the fenestra and anus, and the presence of tubercles surrounding the vulval slit.
TitleSEM of Globodera tabacum perineum
CaptionA scanning electron micrograph of G. tabacum perineum, showing parallel cuticular ridges between the fenestra and anus, and the presence of tubercles surrounding the vulval slit.
CopyrightJanet A. Rowe
A scanning electron micrograph of G. tabacum perineum, showing parallel cuticular ridges between the fenestra and anus, and the presence of tubercles surrounding the vulval slit.
SEM of Globodera tabacum perineumA scanning electron micrograph of G. tabacum perineum, showing parallel cuticular ridges between the fenestra and anus, and the presence of tubercles surrounding the vulval slit.Janet A. Rowe
Potato cyst nematode, Globodera pallida, showing circumfenestrate fenestration, the vulval slit and pattern of cuticular ridges and distance of anus from fenestra.
TitleCircumfenestrate fenestration
CaptionPotato cyst nematode, Globodera pallida, showing circumfenestrate fenestration, the vulval slit and pattern of cuticular ridges and distance of anus from fenestra.
CopyrightJanet A. Rowe
Potato cyst nematode, Globodera pallida, showing circumfenestrate fenestration, the vulval slit and pattern of cuticular ridges and distance of anus from fenestra.
Circumfenestrate fenestrationPotato cyst nematode, Globodera pallida, showing circumfenestrate fenestration, the vulval slit and pattern of cuticular ridges and distance of anus from fenestra.Janet A. Rowe
Potato cyst nematode (Globodera achilleae) from yarrow (Achillea millefolium), from the Compositae group, showing the circumfenestrate fenestration, the anus and type of cuticular patterning.
TitleCircumfenestrate fenestration
CaptionPotato cyst nematode (Globodera achilleae) from yarrow (Achillea millefolium), from the Compositae group, showing the circumfenestrate fenestration, the anus and type of cuticular patterning.
CopyrightJanet A. Rowe
Potato cyst nematode (Globodera achilleae) from yarrow (Achillea millefolium), from the Compositae group, showing the circumfenestrate fenestration, the anus and type of cuticular patterning.
Circumfenestrate fenestrationPotato cyst nematode (Globodera achilleae) from yarrow (Achillea millefolium), from the Compositae group, showing the circumfenestrate fenestration, the anus and type of cuticular patterning.Janet A. Rowe
Scanning Electron Micrograph of the vulva of G. achilleae, which is pore-like as opposed to slit-like and note the absence of tubercles in this area.
TitleSEM of vulva of Globodera achilleae
CaptionScanning Electron Micrograph of the vulva of G. achilleae, which is pore-like as opposed to slit-like and note the absence of tubercles in this area.
CopyrightJanet A. Rowe
Scanning Electron Micrograph of the vulva of G. achilleae, which is pore-like as opposed to slit-like and note the absence of tubercles in this area.
SEM of vulva of Globodera achilleaeScanning Electron Micrograph of the vulva of G. achilleae, which is pore-like as opposed to slit-like and note the absence of tubercles in this area.Janet A. Rowe
The stylet of G. tabacum J2 for comparison with potato cyst nematode J2.
TitleMicrograph of Globodera tabacum
CaptionThe stylet of G. tabacum J2 for comparison with potato cyst nematode J2.
CopyrightJanet A. Rowe
The stylet of G. tabacum J2 for comparison with potato cyst nematode J2.
Micrograph of Globodera tabacumThe stylet of G. tabacum J2 for comparison with potato cyst nematode J2.Janet A. Rowe
Light Micrograph of G. pallida, J2 stylet - note the stylet knob shape.
TitleMicrograph of Globodera pallida
CaptionLight Micrograph of G. pallida, J2 stylet - note the stylet knob shape.
CopyrightJanet A. Rowe
Light Micrograph of G. pallida, J2 stylet - note the stylet knob shape.
Micrograph of Globodera pallidaLight Micrograph of G. pallida, J2 stylet - note the stylet knob shape.Janet A. Rowe
Light Micrograph of G. rostochiensis displaying typical, small, backward sloping stylet knobs.
TitleMicrograph of Globodera rostochiensis
CaptionLight Micrograph of G. rostochiensis displaying typical, small, backward sloping stylet knobs.
CopyrightJanet A. Rowe
Light Micrograph of G. rostochiensis displaying typical, small, backward sloping stylet knobs.
Micrograph of Globodera rostochiensisLight Micrograph of G. rostochiensis displaying typical, small, backward sloping stylet knobs.Janet A. Rowe

Identity

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Preferred Scientific Name

  • Globodera tabacum (Lownsbery & Lownsbery, 1954) Behrens, 1975

Preferred Common Name

  • tobacco cyst nematode

Other Scientific Names

  • Globodera tabacum (Lownsbery & Lownsbery, 1954) Mulvey & Stone, 1976
  • Heterodera tabacum Lownsbery & Lownsbery, 1954

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Nematoda
  •             Class: Secernentea
  •                 Order: Tylenchida
  •                     Family: Heteroderidae
  •                         Genus: Globodera
  •                             Species: Globodera tabacum

Notes on Taxonomy and Nomenclature

Top of page The species Globodera tabacum was first described by Lownsbery, B.F and Lownsbery, J.W. in 1954 from solanaceous plants in Connecticut, USA.

Originally described in the genus Heterodera, it was transferred to the subgenus Globodera by Skarbilovich (1959) and to a separate genus by Behrens (1975). There are at least 12 other species of Globodera, ranging from the best known worldwide pests of potato, G. rostochiensis (Wollenweber, 1923) Behrens, 1975 and G. pallida (Stone, 1973) Behrens, 1975 to the very rare G. leptonepia (Cobb and Taylor, 1953) Behrens, 1975. The genus Globodera consists of species reproducing almost entirely upon solanaceous plants which have radiated from central America and Mexico, with only a few species of solanaceous plants known to be hosts in Old World countries from, for example, the continent of Africa.

Other less common Globodera spp. parasitize members of the Compositae, especially in Asia, and Onagraceae or tree fuchsias in New Zealand. These Globodera species appear to have evolved in separate ecological niches and to have certain biochemical and morphological characters not shared with groups of South or North American origin.

Stone (1983) suggested that G. tabacum (Lownsbery and Lownsbery, 1954) should be considered a species complex, to include G. solanacearum (Miller and Gray, 1972) and G. virginiae (Miller and Gray, 1968) as subspecies.

Description

Top of page Eggs.

Egg length=90-100 µm; Egg width="40"-50 µm.

The eggs are retained in the female's body. After fertilization, the body cuticle toughens and protects the eggs, which stay in-situ until stimulated to hatch. As with most cyst nematodes, this can be for some years. No egg sac is produced.

Juveniles (J2)

Length=500 µm (410-527 µm); Body width at excretory pore=24 µm (22-24 µm); Stylet length=22 µm (19-24 µm); Stylet base to dorsal oesophageal gland duct=5 µm (4.3-6.8 µm); Anus to tail terminus=52 µm (46-59 µm); Hyaline part of the tail=27 µm (23-31µm).

The second-stage, vermiform juvenile hatches from the egg, the moult from first to second stage having been completed before hatching. There are three bands in the lateral field. The head is offset and bears 3-4 head annules. The stylet has three anchor-shaped, anteriorly facing knobs. The stylet conus and shaft are equal in length. One third of the body length is occupied by the oesophageal glands, which overlap the anterior part of the intestine. The median bulb is robust, rounded and approximately 70 µm from the head tip. The excretory pore is about 110 µm from the head tip. The tail is finely pointed and is 50-58 µm long. The hyaline portion of the tail is usually half the tail length.

Female

Stylet length=23 µm (18.5-24 µm); Stylet base to dorsal oesophageal gland duct=5.5 µm (3.8-8.0 µm); Number of head annules=4; Body length (excluding neck)=464 µm (327-688 µm); Body width="310" µm (201-516 µm); Granek's ratio=1.5-2.0; Vulval slit length=9 µm (8-10 µm).

The female has a globose shape when first emerging from the root. At this stage the female is white followed by a yellow to golden phase which lasts until formation of the brown cyst. The head is small and bears four annules. The excretory pore is located at the base of the neck and, if using the SEM, tubercles can sometimes be seen in this region (Mota and Eisenback, 1993a). The mid-body cuticle is covered with zig-zag markings, changing to parallel ridges in the fenestral area. The vulva is contained within an area of thin walled cuticle, having a circumfenestrate fenestration. The vulval slit is approximately 9-10 µm in length, flanked either side by a crescentic arrangement of tubercles, which are both wide and discrete. No underbridge is present. The anus is distinct.

Cyst

Length excluding the neck=550 µm (337-740 µm); Maximum width="500" µm (232-645 µm); Length of fenestra=27 µm (15-32 µm); Width of fenestra=22 µm (15-28 µm); Anus to fenestral edge=35 µm; Length of vulval slit=9-10 µm; Number of ridges=5-10 <14); Granek's ratio=1.5-2.0. No underbridge is present. No bullae present (abullate).

The cyst is globose in shape and lacks a vulval cone. The cuticle is strong and dark brown and the eggs are contained within it. A sub-crystalline layer is usually absent. No underbridge is present. No bullae are present. These characters, together with circumfenestrate fenestration of the vulval area are diagnostic of the genus.

Male

Length=1200 µm (710-1355 µm); a=33; Stylet length=26 µm (24-27 µm); Stylet base to dorsal oesophageal gland duct=4 µm (2.0-3.6 µm); Spicule length=34 µm (26-34 µm); Tail length=4.0 µm (2.0-3.6 µm); Gubernaculum=12 µm.

Males are usually 700-1300 µm in length; the posterior region is twisted through 90° to the remainder of the body. There are four lateral lines at the mid-body, narrowing to two lateral lines both anteriorly and posteriorly. The lateral field extends around the tail terminus. The head is offset and has six head annules. The cephalic framework is robust and heavily sclerotized. The stylet is strong and the three stylet knobs are well developed and rounded, sloping posteriorly. The median bulb is ellipsoidal and prominent, about 95 µm from the head end. The nerve ring is located anterior to the junction of the oesophagus and intestine, where it encircles the oesophagus. The excretory pore is 160 µm from the head end. The oesophageal glands overlap the intestine ventro-laterally. The tail is short and no bursa is present. The gubernaculum is 12 µm long. According to Lownsbery and Lownsbery (1954) a phasmid can be located near the tail terminus. The spicules are approximately 34 µm in length, arcuate and single tipped, which is the normal state for Globodera.

Other measurements can be found in Lownsbery and Lownsbery (1954), Granek (1955), Green (1971), Miller and Gray (1972), Hesling (1973, 1978), Mulvey (1973), Behrens (1975), Mulvey and Golden (1983), Othman et al. (1988), Baldwin and Mundo-Ocampo (1991), Miller (1991), Mota and Eisenback (1993a, b, c).

Distribution

Top of page In the USA, distribution of G. tabacum is limited; the major problem areas are Virginia and Connecticut, from where the tobacco cyst nematodes are beginning to radiate into adjoining States (Melton et al., 1991).

Detailed information for the other countries listed is not available.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaPresentShepherd and Barker, 1990; CABI/EPPO, 2004
JapanPresentUehara et al., 2005
Korea, Republic ofPresentShepherd and Barker, 1990; CABI/EPPO, 2004
PakistanPresentBrown, 1962; CABI/EPPO, 2004

Africa

MadagascarPresentShepherd and Barker, 1990; CABI/EPPO, 2004
MoroccoPresentShepherd and Barker, 1990; CABI/EPPO, 2004

North America

Canada
-QuebecPresentBélair and Miller, 2006
MexicoPresentBecerra and Sosa-Moss, 1976; CABI/EPPO, 2004
USAPresentLownsbery and Lownsbery, 1954; CABI/EPPO, 2004
-ConnecticutPresentCABI/EPPO, 2004
-MarylandPresentCABI/EPPO, 2004
-North CarolinaPresentCABI/EPPO, 2004
-VirginiaWidespreadCABI/EPPO, 2004

South America

ArgentinaPresentChaves, 1993; CABI/EPPO, 2004
ColombiaPresentShepherd and Barker, 1990; CABI/EPPO, 2004

Europe

BulgariaPresentCABI/EPPO, 2004
Former USSRPresentKir'janova, 1963; CABI/EPPO, 2004
FrancePresentShepherd and Barker, 1990; CABI/EPPO, 2004
GreecePresentShepherd and Barker, 1990; CABI/EPPO, 2004
ItalyPresentAmbrogioni and D'Errico, 1995; CABI/EPPO, 2004
SloveniaPresentCABI/EPPO, 2004
SpainPresentCABI/EPPO, 2004
Yugoslavia (former)PresentShepherd and Barker, 1990; CABI/EPPO, 2004

Risk of Introduction

Top of page Measures to stop the introduction of the G. tabacum complex to uninfested areas where tobacco, tomatoes and other solanaceous plants are grown are very important. Many solanaceous plants are hosts of this cyst nematode complex and will act as sources of infestation. The usual precautions of disinfecting boots and equipment should be followed and any waste plant material or contaminated soil must be disposed of in a satisfactory and safe manner.

Host Plants and Other Plants Affected

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Growth Stages

Top of page Seedling stage, Vegetative growing stage

Symptoms

Top of page Tobacco cyst nematodes can cause severe stunting of the aerial parts of tobacco plants and the root system is also much smaller than normal (Milne, 1972). Females and cysts, coloured yellow to dark brown, can normally be seen with the naked eye on infected plant roots, 6 to 8 weeks after planting.

List of Symptoms/Signs

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SignLife StagesType
Leaves / wilting
Roots / cysts on root surface
Roots / reduced root system
Whole plant / dwarfing
Whole plant / early senescence
Whole plant / plant dead; dieback

Biology and Ecology

Top of page The life cycle and the biology of the G. tabacum complex are very similar to those of the potato cyst nematodes, although they have been studied in far less detail. Green and Miller (1969) conducted studies on inter-specific hybridization between G. rostochiensis, G. pallida and all members of the G. tabacum group. F1 progeny were produced but their viability was not tested. The crossing of G. rostochiensis with G. pallida seems to be the most difficult hybridization to achieve, but it is possible (Miller, 1983; Stone, 1983). In the 1970s, G. tabacum, G. virginiae and G. solanacearum were still considered to be separate species but studies with sex attractants showed that interbreeding of the round cyst species from solanaceous hosts was possible (Green and Plumb, 1970). Greet (1972) and Greet and Firth (1977) found little difference in the protein profiles of what is now recognized as the G. tabacum complex. This was substantiated by morphological and hybridization studies (Miller, unpublished; Miller, 1983). Stone (1983) designated G. virginiae and G. solanacearum as subspecises of G. tabacum.

An undescribed species G. 'mexicana' (Campos-Vela, 1967) was also considered to be part of the G. tabacum complex. Golden and Ellington (1972) considered G. 'mexicana' as conspecific with G. tabacum virginiae but Bossis and Mugniery (1993) disagreed. Recent studies, using sophisticated biochemical technology such as two-dimensional gel electrophoresis (Bossis and Mugniery, 1993), rDNA techniques (Thiery and Mugniery, 1996) and other molecular approaches (Thiery et al., 1997), suggest that G. 'mexicana' is very closely related to G. pallida and point out similarities and differences amongst six Globodera species. G. rostochiensis stands apart from the G. tabacum tabacum complex and G. pallida, whereas G. pallida and G. 'mexicana' have many more polypeptides in common than the other combinations of species tested. The hybridization of G. rostochiensis and G. pallida produced juveniles that had stylets more like G. pallida but with lips and oral disc more like G. rostochiensis (Mugniery, 1979). The hybrid juveniles from G. pallida females crossed with G. rostochiensis males were successful in penetrating potato roots but died before moulting. Hybrid crosses between G. rostochiensis females and G. pallida males penetrated potato roots and produced males, which were not fertile. No hybrids were able to reproduce on potato cultivars that were resistant to G. rostochiensis. Miller (unpublished), was able to produce hybrids of potato cyst nematodes with the G. tabacum tabacum complex for many generations.

Host range tests do not always show consistent results, as various combinations of the G. tabacum complex can reproduce on some cultivars of potato (Stelter, 1987; Stone and Miller, 1974) and potato cyst nematodes are capable of reproduction on tobacco (Parrot and Miller, 1977). Stone (1983) also noted that host range is not a reliable indicator of species differences. If hybridization occurs in the field, the resulting genotype may be more able to adapt to its environment than the parent and the 'standard' population would only be conserved in geographically isolated environments.

Within Globodera spp. the first stage juvenile moults inside the egg and the second stage juvenile hatches. Recent experiments by Ambrogioni et al. (1995) on G. tabacum in Italy suggest that at 26°C two generations could be produced on crops of aubergine, each taking around 36 days to complete. At 20°C the time to complete one generation was 72 days and at 30°C the cycle was shortened to 32 days. The maximum number of generations produced on aubergines in Italy is three, whereas in the USA, Barker and Lucas (1984) reported four to five generations from tobacco fields. Globodera tabacum virginiae and G. tabacum solanacerum have temperature requirements and life cycles similar to those reported in Italy (Miller and Gray 1968, 1972).

Glasshouse and laboratory tests showed that black nightshade (Solanum nigrum) a primary host of G. tabacum tabacum (Lownsbery and Lownsbery, 1954) stimulated much greater hatch than Rutgers tomato or tobacco '86-4'. After 10 weeks in pot experiments using the same hosts, S. nigrum and tomato stimulated greater hatch of second-stage juveniles than either tobacco or bare soil (LaMondia, 1995).

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Containers and packaging - woodCysts in soil Yes
Land vehiclesCysts in soil Yes
Plants or parts of plantsCysts in soil Yes
Soil, sand and gravelCysts in soil, water also blown by wind Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Roots adults; cysts; juveniles Yes Yes
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Leaves
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Impact

Top of page G. tabacum tabacum and G. tabacum solanacearum both have the potential to reduce crop yield significantly. In Virginia, USA, in 1983, the state lost $0.7 million due to an estimated yield loss of 15% of tobacco, the most important cash crop in Virginia (Miller, 1986).

In Connecticut, USA, large areas of its' river valley are infested with tobacco cyst nematodes, causing large yield losses and poor quality plants. Nematicides are used extensively in this area and the estimated cost in 1982 was $60,000 per annum (Miller, 1986).

Detection and Inspection

Top of page Females and cysts, coloured yellow to dark brown, can normally be seen with the naked eye on infected plant roots, 6 to 8 weeks after planting.

Similarities to Other Species/Conditions

Top of page Globodera species can be extremely difficult to diagnose and, within each species, variation is common. In particular, the G. tabacum complex and the potato species G. rostochiensis and G. pallida have many morphological features in common which may also overlap in size (for example, female colour, vulval slit length and juvenile body length) and similar host ranges. It is usually necessary to look at more subtle details and values for diagnosis, for example, Granek's ratio, stylet length and stylet knob shape, and the pattern and number of cuticular ridges between the anus and circumfenestrate fenestration of the cyst, which may be circular, parallel or maze-like and are important for species diagnosis.

Globodera species found more commonly on Compositae also have features in common with the tabacum and potato groups, but are sufficiently distinct for them to be distinguished by morphological features such as a very small vulval slit, which appears almost pore-like when viewed using the SEM. It is usually unnecessary to resort to techniques such as biochemical analysis. In species from Compositae, Granek's ratio is generally very small, with a value of 1 or less. Tubercles are not usually present around the vulval region and the anus is typically surrounded by whorl-like ridges of cuticle.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

The control of any cyst nematode is difficult as cysts containing viable eggs can survive in the soil for many years. The build up to large, damaging population densities may require only a single susceptible host crop, depending on the original density and the environmental conditions (e.g. temperature).

In the USA, LaMondia (1996) and Johnson (1995) have conducted many studies into the control and suppression of the G. tabacum complex. Methods used include trap-cropping, chemical control, crop rotation and the use of resistant tobacco genotypes. At the present time there is no information on biological control of the G. tabacum complex.

Trap Cropping

Trap crops have been shown to have a significant effect on G. tabacum reducing populations in both microplots and field plots over three seasons (LaMondia, 1996). The chosen host plants were tobacco, black nightshade (Solanum nigrum) and tomato. The numbers of tobacco cyst nematodes were reduced by 80-96% when the host crop was destroyed after 3-6 weeks.

Chemical Control

Numerous studies have been reported over the last 10 years in the journal Fungicide and Nematicide Tests (e.g. LaMondia, 1993; Johnson, 1988, 1989, 1995; Johnson et al., 1994, 1995; Johnson and Lacks, 1995). Many strategies for control have been suggested, including using chlorpyrifos (Johnson, 1988, 1989; Johnson et al., 1994; Johnson and Lacks, 1995). Control levels of 94% of G. tabacum tabacum were attained with a combination of methyl isothiocyanate, 1, 2-dichloropropane and 1, 3-dichloropropene (LaMondia, 1993).

The continuous cultivation of tobacco in the presence of the tobacco cyst nematode in infested fields is the main cause of crop loss (Komm et al., 1983). All cyst nematodes are reduced if crop rotation with non-hosts is practised. The fact that tobacco is a major cash crop induces commercial growers to forego crop rotation, where the profits are smaller, in favour of reduced yields of tobacco for a higher profit margin. Some cultivated tobacco plants have genotypes which have been identified as resistant to tobacco cyst nematode. Even so, crop losses are still evident when the cyst nematode densities are high. In these situations contact nematicides are applied to reduce the population density to a more manageable level.

Both tobacco cyst nematode susceptible and resistant cultivars are used by growers. Often, they prefer susceptible cultivars as these plants are superior agronomically and the yield is not significantly lower than the with resistant types, particularly when contact nematicides are used. Studies on the effects of alternating resistant and susceptible cultivars and using contact nematicides on tobacco yields and population dynamics of the tobacco cyst nematode have been conducted (Johnson et al., 1989). The most effective measures were the use of the resistant cultivar NC567 and a contact nematicide to reduce cyst nematode population densities, particularly when this combination was used for more than one growing season. In the season following this regime, planting a susceptible cultivar gave the best economic return.

References

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Ambrogioni L; Carppo S; Coniglio D, 1995. Temperature effects on development of Globodera tabacum on eggplant. Nematologia Mediterranea, 23:61-66.

Ambrogioni L; D'Errico FP, 1995. Occurrence of a population of Globodera tabacum in Italy. Nematologia Mediterranea, 23(Suppl):75-79; [^italic~Paper presented at the 5th Congress of the Italian Society of Nematology, Martina Franca (TA), 19-21 Ottobre 1995.^roman~]; 29 ref.

Baldwin JG; Mundo-Ocampo M, 1991. Heteroderinae, cyst and non-cyst forming nematodes. In: Nickle WR, ed. Manual of Agricultural Nematology. New York, USA: Marcel Dekker, 275-362.

Barker KR; Lucas GB, 1984. Nematode parasites of tobacco. In: Nickle WR, ed. Plant and Insect nematodes. New York, USA: Marcel Dekker, 218-242.

Becerra LEN; Sosa-Moss C, 1976. Identification de nematodes fitoparasites (Formadores de Quistes), present en el Valle de Toluca, Estado de Mexico. Tesis Profesional del primer autor. Monterrey, Mexico: Universidad Autonoma de Nuevo Leon.

Behrens E, 1975. Taxonomically useful characters for the differentiation of Heterodera species. Probleme der Phytonematologie. Vortrage anlasslich der 10 Tagung uber Probleme der Phytonematologie im Institut fur Pflanzenzuchtung Gross-Lusewitz der Deutschen Akademie der Landwirtschaftswissenschaften zu Berlin am 11 Juni 1971., 122-142.

Bélair G; Miller S, 2006. First report of Globodera tabacum infecting tobacco plants in Quebec, Canada. Plant Disease, 90(4):527.

Bossis M; MugniTry D, 1993. Specific status of six Globodera parasites of solanaceous plants studied by means of two-dimensional gel electrophoresis with a comparison of gel patterns by a computed system. Fundamental and Applied Nematology, 16(1):47-56; 35 ref.

Brown F, 1962. A Survey of some Plant Parasitic Nematode Problems in Pakistan. Shell International Chemical Company Ltd.

CABI/EPPO, 2004. Globodera tabacum. Distribution Maps of Plant Diseases, No. 929. Wallingford, UK: CAB International.

Campos-Vela A, 1967. Taxonomy, Life Cycle and Host Range of Heterodera mexicana n.sp. (Nematoda: Heteroderidae). PhD. Thesis. Wisconsin, USA: University of Wisconsin.

Chaves E, 1993. A revision of the cyst nematodes from Argentina. Boletin Tecnico Estacion Experimental Agropecuaria Balcarce, 45:113-124.

Cobb GS; Taylor AL, 1953. Heterodera leptonepia n. sp., a cyst forming nematode found in soil with stored potatoes. Proceedings of the Helminthological Society of Washington, 20:13-15.

Golden AM; Ellington DMS, 1972. Re-description of Heterodera rostochiensis (Nematoda: Heteroderidae), with a key and notes on closely related species. Proceedings of the Helminthological Society of Washington, 39:64-78.

Granek I, 1955. Additional morphological differences between the cysts of Heterodera rostochiensis and Heterodera tabacum. Plant Disease Reporter, 39:716 -718.

Green CD Miller LI, 1969. Cyst nematodes: attraction of males to females. Report of Rothamsted Experimental Station for 1968, 1:153-158.

Green CD, 1971. The morphology of the terminal area of the round-cyst nematodes S.G. Heterodera rostochiensis and allied species. Nematologica, 17:34-46.

Green CD; Plumb SC, 1970. The interrelationships of some Heterodera species indicated by the specificity of the male attractants emitted by their females. Nematologica, 16:39-46.

Greet DN, 1972. Electrophoresis and morphometrics of the round-cyst nematodes. Annals of Applied Biology, 71(3):283-286

Greet DN; Firth J, 1977. Influence of host plant on electrophoretic protein patterns of some round-cyst nematode females and use of larvae to obtain less ambiguous results. Nematologica, 23(3):411-415

Hesling JJ, 1973. The estimation of Granek's ratio in round-cyst Heterodera's. Nematologica, 19(1):119-120

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