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© 2005 Plant Management Network.
Accepted for publication 24 November 2004. Published 21 January 2005.


Diagnosis of Trichodorus obtusus and Paratrichodorus minor on Turfgrasses in the Southeastern United States


William T. Crow, Entomology and Nematology Department, University of Florida, P.O. Box 110620, Gainesville 32611


Corresponding author: William T. Crow. wtcr@ifas.ufl.edu


Crow, W. T. 2005. Diagnosis of Trichodorus obtusus and Paratrichodorus minor on turfgrasses in the Southeastern United States. Online. Plant Health Progress doi:10.1094/PHP-2005-0121-01-DG.


Introduction

Nematodes in the family Trichodoridae (Thorne, 1935) Siddiqi, 1961, commonly called "stubby-root" nematodes, are of agricultural importance both as plant-pathogens and as vectors for plant viruses. They are ectoparasites that feed primarily on meristematic cells of root tips. Feeding by these nematodes can cause cessation of root elongation and an abbreviated or "stubby" root system termed stubby root disease (3). The damaged root systems have reduced capacity to extract water and nutrients from soil and predispose turf to environmental stresses.

Two species of stubby-root nematode have been identified as pathogens on warm-season turfgrasses in the southern United States; these are Paratrichodorus minor (Figs. 1 and 2) and Trichodorus obtusus (Figs. 3 and 4) (4,13,14). During the past four years the University of Florida Nematode Assay Lab has conducted nematode diagnosis from approximately 20,000 turfgrass samples. From these turfgrass samples, all of the stubby-root nematodes identified have been either T. obtusus or P. minor. Both species have been demonstrated as pathogens of bermudagrass (Cynodon dactylon and Cynodon hybrids) and St. Augustinegrass (Stenotaphrum secundatum) in greenhouse experiments. However, research shows that T. obtusus is more damaging to both bermudagrass and St. Augustinegrass than is P. minor (4,14). Recently, the University of Florida Nematode Assay lab instituted separate action thresholds for T. obtusus and P. minor on warm-season turf grasses. In order to use separate action thresholds, methods for distinguishing these species were identified that do not require mounting of specimens and can be used with ×100 magnification or less.


 

Fig. 1. Female Paratrichodorus minor.

 

Fig. 2. Male Paratrichodorus minor.


 

Fig. 3. Female Trichodorus obtusus.

 

Fig. 4. Male Trichodorus obtusus.


Disease: Stubby root.

Primary Hosts: Bermudagrass [Cynodon dactylon (L.) Pers. and Cynodon hybrids] and St. Augustinegrass [Stenotaphrum secundatum (Walter) Kuntze].

Pathogens: Trichodorus obtusus Cobb (syn. T. proximus) and Paratrichodorus minor (Colbran) Siddiqi (syn. T. minor, P. christiei).


Symptoms

Aboveground symptoms caused by stubby-root nematodes are similar to those caused by other root-feeding plant-parasitic nematodes on turfgrasses. These symptoms include irregularly shaped patches of wilting (Fig. 5), yellowing, and declining turf (16). In Florida, the turf decline often is accompanied by increased proliferation of weeds. Severe infestations combined with stress conditions can lead to death of the turf (Fig. 6).


 

Fig. 5. Wilting patches of St. Augustinegrass resulting from a high infestation of Trichodorus obtusus.

 

Fig. 6. Dying patches of St. Augustinegrass resulting from a high infestation of Trichodorus obtusus combined with drought stress.


Belowground symptoms are dark and abbreviated or "stubby" root systems (Fig. 7), hence the names stubby root disease and stubby-root nematode. However, these symptoms are indistinguishable from those caused by other virulent ectoparasitic nematodes such as sting nematode (Belonolaimus longicaudatus).


 

Fig. 7. Roots of St. Augustinegrass grown in soil inoculated with Trichodorus obtusus (left) and in uninoculated soil (right).

 

Host Range

Known hosts of T. obtusus are: bermudagrass (4), St. Augustinegrass (4,14), and tomato (Lycopersicon esculetum) (9). It has been associated with big bluestem (Andropogon gerardi), sideoats grama (Bouteloua curtipendula), Eucalyptus sp., Kentucky bluegrass (Poa pretensis), rhododendron (Rhododendron sp.), sabal palm (Sabal palmetto), potato (Solanum tuberosum), littleleaf linden (Tilia cordata), sweetbay magnolia (Magnolia virginiana) (12), sorghum-sudangrss (Sorghum bicolor × S. arundinaceum) (9), and seashore paspalum (Paspalum vaginatum) (10).

Paratrichodorus minor has over 100 known hosts (5). Turfgrass hosts include bermudagrass, St. Augustinegrass, annual bluegrass (Poa annua), Italian ryegrass (Lolium multiflorum), perennial ryegrass (L. perenne) (2), and creeping bentgrass (Agrostis palustris) (15).


Geographic Distribution

Trichodorus obtusus is only known to occur in the United States. A report of T. proximus (a synonym of T. obtusus) from Ivory Coast (1) was later determined to be a different species (6,8). Within the United States it has been reported in the states of Virginia, Florida, Iowa, Kansas, Michigan, New York, and South Dakota (6,12). The author found T. obtusus infesting St. Augustinegrass lawns near Dallas, Texas.

Paratrichodorus minor is spread around the globe, being reported in Afghanistan, Argentina, Belgium, Brazil, Canary Islands, Cuba, Egypt, Fiji, India, Israel, Italy, Ivory Coast, Japan, Java, Mauritania, Netherlands, New Zealand, Nicaragua, Philippines, Portugal, Puerto Rico, Russia, Senegal, Sweden, Switzerland, Taiwan, United States, Upper Volta, Venezuela, and West Germany (5). Within the United States it is widespread, being reported in most states (12).


Pathogen Isolation

As ectoparasites, stubby-root nematodes are extracted from soil rather than plant tissue. The University of Florida Nematode Assay Lab has had good success extracting both T. obtusus and P. minor using either centrifugal-flotation or Baermann funnel techniques. However, any of the common methods for extracting nematodes from soil may probably be used (11).


Pathogen Identification

The Trichodoridae are the only plant parasites in the order Triplonchida. Triplonchida have a two-part esophagus made up of a narrow anterior region expanding gradually to a swollen muscular base (Fig. 8). However, because the esophagus of trichodorid nematodes often overlaps the intestine and the basal portion expands gradually with no clear distinction between the anterior and basal regions, it is often difficult to distinguish the esophageal shape (Fig. 9). The key morphological feature used to distinguish the Triplonchida from other orders, a six-layer cuticle, is typically not seen except with high-quality mounted specimens and is not a useful feature in most diagnostic settings.


 

Fig. 8. The anterior region of Trichodorus obtusus. In this occurrence, the swollen muscular basal portion and narrow anterior region are easily observed. The curved onchiostyle also is clearly visible.

 

Fig. 9. The anterior region of Paratrichodorus minor. In this common occurrence, the esophageal shape of stubby-root nematodes is difficult to distinguish. However, the curved onchiostyle is clearly visible.


The most useful feature in the identification of Trichodoridae in diagnostic settings is their onchiostyle, a solid, dorsally curved stylet (Figs. 8 and 9) exclusive to the Trichodoriae that is clealy visible at ×25 magnification (Figs. 1 to 4). The only other stylet-bearing nematodes in the order Triplonchida are the fungivorous Ditherphoridae which have a convoluted or complex stylet (Fig. 10). Body shape is another useful morphological feature in identification of Trichodoridae. The body shape of the Trichodoridae is usually described as "cigar-shaped," meaning its body width to length ratio is high and is more or less rounded at both ends (Figs. 1 to 4).


 

Fig. 10. The anterior region of Diptheropthora sp. The stylet of Dipheropthora is convoluted or complex.

 

The genera Trichodorus and Paratrichodorus are separated from the other genera in the Trichodoridae, Monotrichodorus and Allotrichodorus, by the number of gonads present in the females. In Trichodorus and Paratrichodorus females are amphidelphic, meaning they have two genital tracts facing in opposite directions (Figs. 11 and 12), whereas in Monotrichodorus and Allotrichodorus females are monodelphic-prodelphic, meaning there is a single genital tract stretching anteriorly.


 

Fig. 11. The female reproductive tract of Trichodorus obtusus is paired, with each pair facing opposite directions. The vagina is barrel-shaped and sclerotized.

 

Fig. 12. The female reproductive tract of Paratrichodorus minor is paired, with each pair facing opposite directions. The vagina is oval in shape and not sclerotized.


In the case of warm-season turfgrasses in the southeastern United States the only species of stubby-root nematodes commonly associated with turf are T. obtusus and P. minor. Therefore, in a turgrass diagnostic setting, distinguishing between these two species is all that is necessary in the majority of cases. Fortunately, T. obtusus and P. minor are easily distinguished from each other.

The presence or absence of males and the morphology of male sexual organs are the most useful features for separating T. obtusus from P. minor in a diagnostic setting. Trichodorus obtusus is an amphimictic species; both sexes are required for reproduction. Generally T. obtusus males are abundant in a given population. Contrarily, P. minor reproduces parthenogenically, and since males are not needed for reproduction they are very rare. Males of T. obtusus have no bursa (caudal alae) and the spicules are large and curved (Fig. 13). If males of P. minor are present, a small bursa is present, and the spicules are thin and fairly straight (Fig. 14). Males of T. obtusus have 3 supplementary organs (precloacal ventromedian supplements) that are readily visible at ×400 or less (Fig. 13), whereas P. minor has only one that is so small it is not normally seen using light microscopy (Fig. 14).


 

Fig. 13. The posterior of a male Trichodorus obtusus. The spicules are large and curved, and no bursa is present. Three supplementary organs are located anterior to the base of the spicules.

 

Fig. 14. The posterior of a male Paratrichodorus minor. The spicules are reduced and a bursa is present. Supplementary organs are not visible.


Body length also is a very useful characteristic that can be used to separate T. obtusus from P. minor. Trichodorus obtusus is a larger nematode than P. minor. Paratrichodorus minor has female body lengths close to 500 µm (10), whereas female body lengths of T. obtusus are 1100 to 1500 µm (4). Female sexual organs also may be used in distinguishing T. obtusus from P. minor but are less useful in diagnostic settings than are male characteristics. The vulva of T. obtusus is barrel-shaped when relaxed, sclerotized, and easily seen (Fig. 11). The vulva of P. minor is oval-shaped, less sclerotized, and not seen as easily (Fig. 12).

Occasionally other Trichodorus or Paratrichodorus species may be present in turfgrass samples, making it necessary to separate T. obtusus or P. minor from other nematodes within the same genus. Trichodorus obtusus is distinguished from other Trichodorus spp. found in the United States by having a single ventromedian cervical pore located slightly anterior to the excretory pore in the esophageal region of the male nematode (Fig. 15), other species in the United States have multiple ventromedian cervical pores. All three supplementary organs of T. obtusus males are typically located anterior to base of the spicules (Fig. 13), other Trichodorus spp. found in the United States have either no supplementary organs or at least one that is not anterior to the base of the spicules. Females of T. obtusus typically have a barrel-shaped vagina when relaxed (Fig. 11), while vagina of other species are shaped otherwise. Paratrichodorus minor is distinguished from other Paratrichodorus spp. species by the females having no lateral body pores, the vulva a transverse slit, and an oval-shaped vagina (Fig. 12). Some useful diagnostic keys to species of Trichodorus and Paratrichodorus are available by W. Decreamer (5,7).


 

Fig. 15. A male Trichodorus obtusus. A single ventromedian cervical pore is located anterior to the excretory pore.

 

In summary, stubby-root nematodes are identified primarily on the presence of a curved onchiostyle and "cigar-shaped" body. On warm-season turfgrasses in the southeastern United States T. obtusus and P. minor are the most common species of stubby-root nematodes, and may be separated based on the following features. Trichodorus obtusus is generally > 1 mm long and has abundant males with large curved spicules, 3 supplementary organs anterior to the spicule base, no bursa, and a single ventromedian cervical pore immediately anterior to the excretory pore. Paratrichodorus minor is close to 0.5 mm long, mostly females, and males (if present) have a small bursa, straight spicules, and no visible supplementary organs or ventromedian cervical pore.


Literature Cited

1. Baujard, P. 1983. Observations sur les Trichodoridae Thorne, 1935 (Nematoda) de l’Afrique de l’Ouest. Rev. Nematol. 6:223-228.

2. Bell, N. L., and Watson, R. N. 2001. Identification and host range assessment of Paratylenchus nanus (Tylenchida: Tylenchulidae) and Paratrichodorus minor (Triplonchida: Trichodoridae). Nematology 3:483-490.

3. Christie, J. R., and Perry, V. G. 1951. A root disease of plants caused by a nematode of the genus Trichodorus. Science 113:491-493.

4. Crow, W. T., and Welch, J. K. 2004. Root reductions of St. Augustinegrass (Stenotaphrum secundatum) and hybrid bermudagrass (Cynodon dactylon × C. Transvaalensis) induced by Trichodorus obtusus and Paratrichodorus minor. Nematropica 34:31-37.

5. Decreamer, W. 1991. Stubby root and virus vector nematodes. Pages 587-625 in: Manual of Agricultural Nematology. W. R. Nickle, ed. Macel Dekker, Inc. New York.

6. Decreamer, W. 1995. The family Trichodoridae: Stubby root and virus vector nematodes. Kluwar Academic Publishers, Dordrecht, Netherlands.

7. Decreamer, W. 1980. Systematics of the Trichodoridae (Nematoda) with keys to their species. Rev. Nematol. 3:81-99.

8. De Waele, D. 1986. Taxonomic remarks concerning Trichodorus proximus Allen, T. eburneaus De Waele & Carbonell and T. coomansi De Waele & Carbonell (Nematoda: Trichodoridae). Nematologica 32:115-117.

9. Harrison, R. E. 1975. The corky ringspot disease of potatoes: Biology of Trichodorus christiei and Trichodorus proximus and evidence of unstable tobacco rattle virus in corky ringspot-infected potatoes. Ph.D. dissertation. University of Florida, Gainesville, FL.

10. Hixson, A. C., and Crow, W. T. 2004. First report of plant-parasitic nematodes on seashore paspalum. Plant Dis. 88:680.

11. McSorley, R. 1987. Extraction of nematodes and sampling methods. Pages 13-47 in: Principles and Practice of Nematode Control in Crops. R. H. Brown and B. R. Kerry, eds. Academic Press Australia, Marrickville, Australia.

12. Noffsinger, E. M. 1984. Family Trichodoridae. Pages 20-29 in: Distribution of Plant-Parasitic Nematode Species in North America. Soc. Nematol., Hayattsville, Maryland.

13. Rhoades, H. L. 1962. Effects of sting and stubby-root nematodes on St. Augustine grass. Plant Dis. Rep. 46:424-427.

14. Rhoades, H. L. 1965. Parasitism and pathogenicity of Trichodorus proximus to St. Augustine grass. Plant Dis. Rep. 49:259-262.

15. Sikora, R. A., and Taylor, D. P. 1974. Pathogenicity of Trichodorus christiei to creeping bentgrass. Meded. Fac. Landbouwwet. Rijksuniv. Gent 39:1,713-718.

16. Smiley, R. W., Dernoeden, P. H., and Clarke, B. B. 1992. Compendium of Turfgrass Diseases, 2nd ed. American Phytopathological Society, St. Paul, MN.