Alfalfa stem nematode, Ditylenchus dipsaci, root-knot nematode, Meloidogyne spp. and lesion nematodes, Pratylenchus spp. are major constraints responsible for yield reduction in alfalfa production. Though the above ground symptoms caused by these nematodes are almost similar, management strategies developed against each varied depending on the mode of habitat and duration of their survival in soil and root. Management of stem nematode involves prevention, use of resistant varieties and cultural practices followed by application of chemical nematicides, while the success of root-knot and lesion nematode control involves utilization of rotational crops and chemicals for the effective management. Manipulation of resistant varieties against all of the above nematodes considerably reduces the nematode damage with a subsequent increase in yield at field level.

Key words: Alfalfa, Ditylenchus dipsaci, Meloidogyne spp., nematode management, Pratylenchus spp.

Plant parasitic nematodes are one of the major constraints on irrigated alfalfa production. Among all, alfalfa stem nematode (Ditylenchus dipsaci), root-knot nematode (Meloidogyne spp.) and root lesion nematode (Pratylenchus spp.) are predominantly distributed in Pacific northwest regions. Direct damage to alfalfa roots and stems leads to susceptibility of the plant to other pathogenic bacteria and fungi. Nematode infection not only reduces alfalfa seed and hay yields, but also shows major impact on other crops grown in rotation with alfalfa. Some nematode, such as dagger, needle and stubby root nematodes are also more important as they are potential agents for the virus vector rather than for causing damage on alfalfa. To develop an effective management tactic, it is essential to know the distribution, biology and impact of other abiotic factors on nematode life cycle at field level. Hence, distribution of major nematode pests on alfalfa in Idaho, their life cycle, symptoms and impact on alfalfa yield is dealt with here followed by an efficient management strategy at field level.

1. ALFALFA STEM NEMATODE, DITYLENCHUS DIPSACI

Distribution and Host Range

In Idaho and other northwestern states, the alfalfa stem nematode has been found in many alfalfa producing areas. It is the most serious yield-limiting nematode in Idaho and other alfalfa producing areas around the world. The alfalfa stem nematode prefers heavy soils and high water inputs (from rainfall or irrigation), and it is often found in areas where irrigation waste water is used. Although stem nematodes as a group parasitize over 450 different plant species including alfalfa, garlic, potatoes, and beets, they occur in several biological "races" that have limited host ranges. The alfalfa race can parasitize several plant species, but it reproduces only on alfalfa and seedlings of sainfoin (another legume hay). The alfalfa race apparently can also reproduce on potato, but not on onion.

Life Cycle, Survival, and Dissemination of the Stem Nematode

Stem nematodes are one of the few groups of nematodes that feed mainly on above ground plant parts and rarely on roots. After emerging from eggs, all stages of the stem nematode are able to attack the alfalfa plant. A mature female lives 45 to 73 days, reproduces sexually, and generates 200 to 500 eggs during her lifetime. Under average summer temperatures and adequate moisture conditions, the life cycle is completed in 19 to 30 days.

Although alfalfa stem nematode adults and eggs overwinter in succulent alfalfa tissue in the crown of the plant or in soil, the fourth stage larvae are the most likely to survive unfavorable conditions and re-infect plant tissue. The alfalfa stem nematode also overwinters in crop debris, seed, hay, and in association with susceptible weed hosts. Although stem nematodes can be found in soil, they usually enter the soil only if conditions become unfavorable in plant tissue. Compared to other plant parasitic nematodes, stem nematodes are unique in that they can withstand dehydration for long periods of time. The alfalfa stem nematode can be introduced into clean fields through uncleaned infested seed or other plant tissue (historically one of the most important means of stem nematode dissemination), contaminated manure and irrigation water, and harvesting equipment.

Symptoms Caused by the Stem Nematode

Field symptoms usually appear as patches of poor, stunted growth, and bare patches where weeds can invade. Nematodes feeding on plants in winter cause most of the damage, which becomes apparent the following spring.

• Infested areas show poor growth in spring.
• Severely infected plants may die, and if wet weather persists, entire stands may be lost.
• Infected buds become swollen and distorted, and they are unable to elongate into normal stems. Depending on variety, significant yield losses may occur due to shortened internodes.
• Under warm, humid conditions, alfalfa stem nematodes may migrate into the leaf tissue and kill chloroplasts. The infected leaf tissue then turns white, and the resulting symptom is referred to as "white flagging".
• Infection of the flower buds may lead to contaminated seed. Up to 17,000 alfalfa stem nematodes have been recovered from one pound of uncleaned seed.
• The alfalfa stem nematode occasionally feeds on roots, and root symptoms include internal cavities or gall-like outgrowths that may girdle the root crown.

The alfalfa stem nematode can vector the bacterial wilt pathogen, Clavibacter michinganense subsp. insidiosum, and has been implicated in breaking resistance to bacterial wilt in resistant or tolerant varieties of alfalfa. Alfalfa stem nematode can potentially cause more severe damage in the presence of other foliar fungal diseases, such as black stem and leaf spots.

Impact of Alfalfa Stem Nematode on Yield

Damage by the alfalfa stem nematode usually occurs before the first cutting during cool, humid weather. Nematodes in alfalfa stems may be removed with the first cutting, reducing the danger of infection during later cuttings. However, later cuttings may also become infected if soil is wet, since nematodes require water to migrate to infection sites.

Alfalfa varieties considered to be generally resistant to alfalfa stem nematode include "Washoe", "Lahontan", and "Archer". Alfalfa varieties vary in their levels of resistance to alfalfa stem nematode. In a greenhouse evaluation conducted in 1986, four commercially available varieties of alfalfa ("Apollo II", "Lahontan", "Ranger", and "Washoe") and two experimental varieties were evaluated for their yield response to alfalfa stem nematode in greenhouse experiments. To measure dry matter, five cuttings were obtained throughout the duration of the experiment. Reductions in total herbage weight occurred for all varieties when they were inoculated with alfalfa stem nematode, but "Washoe" experienced the smallest yield loss (Table 1).

Management Strategies for Alfalfa Stem Nematode

Resistant varieties

Planting varieties with high levels of resistance, such as "Archer", "Lahontan", and "Washoe" is probably the best management tool available, especially when alfalfa is grown in irrigated land. It has been suggested that without some level of stem nematode resistance, alfalfa production would be seriously threatened in many areas.

Prevention

• Use clean, nematode-free seed.
• Avoid moving contaminated farm machinery or livestock from an infested field to a clean field.
• Avoid using contaminated waste water or tail water.
• Keep manure from feedlots where cattle have been fed infected hay out of clean fields.

Cultural practices

• Fall burning (in alfalfa seed production systems) decreases nematode infection and mortality, but spring burning appears to enhance infection and increase plant mortality.
• The alfalfa stem nematode is a biological "race" of stem nematodes, and its host range is very limited. Consequently, rotation with nonhost crops such as sorghum, small grains, beans, and corn on a 2- to 4-year basis should reduce alfalfa stem nematode populations. Be careful to avoid re-infesting the field with contaminated irrigation water or machinery. Eliminating old and volunteer alfalfa plants through a weed control program is also important to avoid re-infestation.
• Cutting alfalfa fields only when the top 2 to 3 inches of soil are dry should help reduce reinfection. University of Idaho variety trials demonstrate that frugal applications of irrigation water to keep soil surfaces dry will minimize spread into later cuttings.

Chemical control

• No nematicides are registered for use against the alfalfa stem nematode.
• Fumigation before planting may be costly relative to potential economic benefits.

2. ROOT KNOT NEMATODES, MELOIDOGYNE SPECIES

Distribution and Host Range

Root knot nematodes are among the most widespread and economically important of plant parasitic nematodes. In Idaho, two species of economic concern are the northern root knot nematode (M. Hapla) and the Columbia root knot nematode (M. Chitwoodi). The northern root knot nematode is distributed throughout Idaho and the United States, while the Columbia root know nematode occurs in the Columbia River Basin of Washington and Oregon, in Idaho and northern California, and in parts of Nevada. Though found in most soil types, they are most abundant in sandy loam soils. Root knot nematodes on alfalfa are of economic concern partly for the direct damage they can cause, but more importantly for the serious damage they inflict on high value susceptible crops that are grown in rotation with alfalfa such as potato, sugarbeet, and bean.

Root knot nematodes have wide host ranges. The northern root knot nematode attacks over 550 different hosts, including alfalfa. Grain crops, however, are poor hosts for the Northern root knot nematode. In contrast, grains (specifically wheat and barley) are hosts for the Columbia root knot nematode. Two races of the Columbia root knot nematode, race 1 and race 2, occur in Idaho, but only race 2 is able to reproduce on susceptible alfalfa varieties.

Other species of root knot nematode that are plant parasitic on alfalfa (M. Arenaria, M. incognita, and M. javanica) do not survive in Idaho, since they are not adapted to low winter temperatures.

Life Cycle, Survival, and Dissemination of Root Knot Nematodes

Unlike the stem nematode which infects plant tissue during all stages in its life cycle, root knot nematodes are infectious only when they are newly hatched second stage juveniles. After entering the root, second stage juveniles undergo three more molts. As the alfalfa seedling develops, second stage juveniles which penetrated root tissue become established and sedentary in the cortical tissue. Feeding of the nematode initiates a series of host responses, culminating in the formation of galls, and giant plant cells within the galls provide food for the nematodes. As females mature, their bodies swell and they remain immobile. Pearly white swollen females, about the size of a pinhead, can be seen. Root knot nematodes reproduce sexually, and mature females deposit 50 to 1000 eggs in a gelatinous matrix within root tissue. Males maintain their long and slender body, and after the fourth molt, they are once again mobile. Under ideal conditions, the life cycle of root knot nematodes is usually completed in 20 to 25 days, and four to five generations may occur in one growing season. For M. hapla, the life cycle on alfalfa takes approximately 30 days at 77^oF. Root knot nematodes overwinter as second stage juveniles and as eggs in the soil. They may also survive as egg masses in root tissue from the previous crop.

Symptoms Caused by Root Knot Nematodes

Infection of alfalfa by Meloidogyne species may be confined to localized areas of a field or extend throughout an entire field. The extent of the damage in the field depends on several factors, including initial nematode population level, alfalfa variety, and soil temperature at planting time. High initial populations and warm soil temperatures may cause serious injury to seedlings, resulting in stunting.

The northern root knot nematode infects and parasitizes roots of alfalfa plants and causes the plant cells to enlarge into small oval galls on the roots that can be seen with the naked eye. Galls caused by root knot nematodes are accompanied by lateral root growth, unlike galls caused by the beneficial nitrogen-fixing bacteria. In a heavily infested field, young seedlings may be killed by this nematode, even though roots may not display galls. The Columbia root knot nematode (race 2) produces similar symptoms as the northern root knot nematode, but it is less pathogenic to alfalfa, and they cause tiny galls that can easily be missed if roots are not examined carefully.

Root knot nematodes, like stem nematodes, are implicated in interactions with other pathogens. Bacterial wilt, Phytophthora root rot, Fusarium wilt, and damage by the alfalfa stem nematode may be enhanced on alfalfa when the northern root knot nematode is present.

Impact of Root Knot Nematodes on Yield

A greenhouse experiment was conducted to evaluate the response of four commercial alfalfa varieties and two experimental varieties to infection by the northern root knot nematode. Dry matter weight data were obtained for each variety from inoculated and non-inoculated plants, and five cuttings were taken over the course of the experiment. Results suggest that yield reductions are influenced by cultivar resistance levels (Table 1).

In a separate greenhouse experiment, the effect of various commercial alfalfa cultivars on population density of the Columbia root knot nematode was evaluated. Lobo, Archer, and Nevada Syn-XX reduced populations of the Columbia root knot nematode by 92, 89, and 77%, respectively, compared to the susceptible cultivar Lahontan.

Management of Root Knot Nematodes

Resistant varieties.

Use of resistant alfalfa varieties is probably the most practical means of managing root knot nematodes. A number of resistant varieties are now commercially available.

Crop rotation.

Crop rotation to manage the root knot nematode is not very successful because of the wide host range of these nematodes.

Chemical control.

Soil fumigation before planting can be effective against the northern root knot nematode. However, fumigants are expensive and they are generally not economically feasible on alfalfa. No non-fumigant nematicides are currently registered on alfalfa.

3. ROOT LESION NEMATODES, PRATYLENCHUS SPECIES

Distribution and Host Range

Root lesion nematodes are found throughout the world in temperate and tropical regions. Like root knot nematodes, lesion nematodes have a wide host range that varies from crops to weeds, and they are most destructive to roots of cultivated and non-cultivated plants in sandy or sandy loam soils. Many species of root lesion nematodes are associated with alfalfa. The most economically important species of lesion nematode is Pratylenchus penetrans, but this species is relatively uncommon in Idaho. The most common species in Idaho are P. neglectus and P. thornei.

Life Cycle, Survival, and Dissemination of Root Lesion Nematodes

Pratylenchus species are migratory, endoparasitic nematodes that can invade plant roots at all stages of the life cycle outside the egg (similar to the stem nematode). As in the stem and root knot nematodes, second stage juveniles of root lesion nematodes emerge from eggs (nematodes typically undergo their first molt inside the egg). Lesion nematodes penetrate the entire root system, except root tips, by forcing their way between or through epidermal and cortical cells. They feed on cell contents as they migrate within roots. Females deposit eggs in root tissue or soil, and the eggs in plant tissue or in soil survive winters. Females do not survive winters in Idaho. The most important method of dissemination of root lesion nematodes is probably contaminated irrigation water, machinery, or tare dirt.

Symptoms of Root Lesion Nematodes

Plants infected with root lesion nematodes do not show above ground symptoms that can positively aid in nematode identification. Above-ground symptoms are more general, and can include stunting and nutrient deficiencies. Root lesion nematodes reduce root growth and inflict black or brown lesions on the root surface. Lesions may fuse to cause the entire roots to appear brown. Secondary infections of roots by other bacterial and fungal pathogens commonly occur after root lesion nematode invasion. Alfalfa resistance to these secondary pathogens may sometimes be overcome due to root lesion nematode invasion.

Impact of Root Lesion Nematodes on Yield

In a greenhouse experiment conducted at Parma, three commercial varieties and two experimental varieties were evaluated for their response to root lesion nematode infection. Variety dry matter weights were obtained from inoculated and non-inoculated plants. Five cuttings were taken over the course of the experiment. Root lesion nematode significantly reduced dry matter for all varieties compared to non-inoculated treatments (Table 2). However, yield reductions for the experimental varieties were lower than three commercially available varieties (Baker, Ranger, and Nevada Syn-XX). The development of alfalfa varieties that display root lesion resistance and agronomically desirable characteristics is on-going.

Management of Root Lesion Nematodes

Crop rotation.

Since lesion nematodes have a very wide host range, and more than one species may occur in a field, crop rotation is not effective for lesion nematode management. However, leaving a field fallow, followed by treatment with a nematicide, can reduce lesion nematode populations.

Resistant varieties.

Scientists in Idaho and Minnesota have identified and developed alfalfa germplasm with resistance to lesion nematodes. However, alfalfa varieties with adequate resistance are not yet commercially available. When varieties with satisfactory resistance to one or more Pratylenchus species become available, they will probably be the best means of controlling lesion nematodes since the cost of chemical control is prohibitive.

Table 1. The effect of alfalfa stem nematode or northern root knot nematode on yield reduction of different alfalfa varieties. Data represents weighted means of five dry matter yield cuttings under greenhouse conditions (Parma, ID, 1986).

	Average Yield Reduction (%)*
Variety	Stem Nematode	Northern Root Knot Nematode
Ranger	12.8 a	2.2 bc
EXP 49	7.3 b	-2.6 d
EXP 107	7.0 b	0.6 cd
Lahontan	7.7 b	5.5 a
Apollo II	7.1 b	0.3 cd
Washoe	5.5 c	4.2 ab
*LSD (0.10) was used for mean separations. Values within columns followed by the same letter are not significantly different.

Table 2. The effect of lesion nematode, Pratylenchus penetrans, on foliar weight of different alfalfa varieties under greenhouse conditions.

Variety	Average Yield Reduction (%)*
AP 8831	16.1 b
AP 8821	15.0 b
Baker	23.1 a
Ranger	22.0 a
Nevada Syn-XX	23.1 a
*LSD (0.10) was used for mean separations. Values followed by the same letter are not significantly different.

Hanson, A.A., D.K. Barnes, and R.R. Hill, Jr., eds. Alfalfa and alfalfa Improvement. American Society of Agronomy, Crops Science Society of America, and Soil Science Society of America: Madison, WI.

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¹S. Hafez, Extension Nematologist, University of Idaho, Parma R&E Center, 29603 U of I Lane, Parma, ID, 83660. Published In: Proceedings, 28^th California/Nevada Symposium, December 3-4, 1998, Reno, NV.