Introduction to Plant Parasitic Nematodes and Their Management Jimmy R. Rich and Stanley B. Hendley IFAS/NFREC University of Florida

Nematodes Human Parasitic Insect Parasitic Plant Parasitic Phylum Nematoda Roundworms Microbial Feeders (90% plus) Animal Parasitic Human Parasitic Insect Parasitic Plant Parasitic Nematodes – Nematodes are small, mostly microscopic, nonsegemented roundworms. However, sizes range widely, and animal parasitic nematodes are generally largest. The vast majority of nematodes are beneficial microbial feeders and reside in the soil. They help promote healthy soil environments, that includes nutrient recycling. Other nematodes, such as insect feeders, provide benefits through reduction in populations of insects, e.g. mosquitoes, that are harmful to plants, animals and man. (The drawing shows the morphology of a typical plant-parasitic nematode. Note that some nematodes swell and are not vermiform (wormlike) during parts of their life cycle. This drawing is of a ‘ring’ nematode, it is widely found and quite damaging in golf courses and home lawns.

Interesting Facts Most numerous animal Second most numerous species Size: mostly microscopic Longest is 26 feet (in Blue whale) Simple morphology No circulatory system No respiratory system No skeleton Interesting Facts – Nematodes are estimated to be the most numerous animals in the world, even more than insects. To paraphrase one eminent nematologist, he said ‘should everything else on earth disappear except nematodes, their would still be a dim outline of all that had been present. (Note the scanning electron micrographs of, in this case, a plant-parasitic nematode – 1. Upper right, the cuticle (skin) of a nematode with the typical lateral line and annules (rings) on the body; 2. A male nematode tail with reproduction organs – spicules; 3. Face view showing the opening where the stylet (spear) protrudes for plant feeding).

Examples of Non-Plant-Parasitic Nematodes Animal Parasites Canine heart worms, Ascaris Human Parasites pinworms, hookworms Insect Parasites mosquitoes, mole crickets, citrus weevils Examples – Most people can relate to nematodes found in their pets and those sometimes found in humans. However, these are seldom called ‘nematodes’ but rather ‘parasites, helminthes, roundworms, etc. Dog heartworms, for example, are nematodes and transmitted by mosquitoes. Human nematode parasites affect upwards of ½ billion people worldwide. Some insect parasitic nematodes are now commercially available and provide safe and effective control of insects. The photo at the upper right shows nematodes infecting grasshoppers – the nematodes can be seen with the naked eye and appear as ‘strings’. Below are mosquito larvae infected with nematodes.

Plant-Parasitic Nematodes Over 6000 known species Present in all ecological niches Attacks almost all plants Cause 10% losses to crops Reduces ornamental growth Serious turf problems Big problem on tree crops Plant Nematodes – The study of plant-parasitic nematodes is relatively young compared to study of plant diseases and insects. Thus, there is still very much to be learned. However, we know that nematodes parasitize a huge number of plants (if not all) and cause billions of dollars worth of damage to world food crops as well as tree crops, turf and ornamentals. Damage or potential damage from nematodes must always be considered when producing plants. (The photos show palm trees declining with eventual death from the ‘red ring’ nematode disease. The nematodes are transmitted by the palm weevil.

Morphology A nematode has: Digestive organs Reproductive organs Excretory structures Muscles Nerves Tough skin or “Cuticle” Morphology – Nematodes have a more detail structure than shown here. However as indicated, they possess no circulatory, respiratory or skeletal systems. Body ‘structure’ is maintained by fluid that surrounds the organs in the body cavity (pseudocoelom). As a result of no skeletal structure, nematodes must always be surrounded in a film of water or other liquid to prevent body collapse from drying and resultant death. Hence, do not allow nematode soil samples to dry out!

Plant-parasitic nematodes all have stylets (spears) that penetrate cells and withdraw the contents. Stylet – Plant-parasites possess a stylet (spear) which differentiates them from other groups of nematodes. The stylet is used to puncture plant cell walls and membranes to allow withdrawal of cell contents. Stylets of most plant nematodes are hollow which provides a channel for cell contents to pass. A few have solid stylets that contain groves on the outside for this purpose. The general feeding process is: 1) the stylet pierces a cell; 2) digestive glands (esophageal glands) discharge enzymes which partially dissolve cell contents; then 3) contents are sucked by the action of the pumping bulb (median bulb) into the intestines (no stomach).

Nematode Names Plant nematodes have both common and scientific names, some of economical importance, by common name, are: Root-knot, Sting, Stubby-root, Reniform, Lance, Ring, Lesion, Burrowing, Citrus, Spiral, and Cyst Nematode Names – Plant nematodes are generally given common names according to either damage symptoms they produce on plants or some striking morphological feature they possess. For example, root-knot nematodes produce root ‘knots’ while stubby root nematodes cause ‘stubby’ looking roots. The cuticle of ring nematodes looks like a stack of coins giving it a ‘ringed’ appearance, while lance nematodes have a robust stylet, resembling a ‘lance’.

Feeding Habits Nematodes may be grouped by feeding habit as: Endoparasitic– entire body inside the root Ectoparasitic– entire body outside the root Semi-endoparasitic- part of body inside root By movement when feeding, they are called: Sedentary – mostly immobile during their life Migratory – mobile for all their life. Feeding Habits. Nematode feeding habits are described according to whether they feed inside or outside a root and if they move or not while feeding.

Feeding Habits of Some Plant-parasitic Nematodes Root-knot Feeding Habits –Root-knot nematodes are sedentary and endoparasitic while the lesion nematode is migratory and endoparasitic. Note that the root-knot nematodes swell and appear pear-shaped, and thus, become sedentary. Lesion

Feeding Habits of Some Plant-parasitic Nematodes Cyst Ring Feeding Habits – Cyst nematodes are sedentary and semi-endoparasitic while ring nematodes are sedentary and ectoparasitic.

Feeding Habits of Some Plant-parasitic Nematodes Stubby root Feeding Habits – The stubby-root nematode is migratory and ectoparasitic while reniform nematodes are sedentary and semi-endoparasitic. Most nematodes initiate feeding just behind tips of young roots. However, some like the stubby-root nematode feed directly on the root tip, generally preventing further root elongation – hence stubby roots. Reniform

Nematode Damage Nematodes damage plants by reducing or modifying root mass Root cells are killed or modified to serve as food for the nematode Typical root and foliar symptoms result Nematode Damage – Nematode damage is mainly a function of reduction of plant root mass. The feeding activities of most plant nematode result in plant root destruction, thereby limiting water and nutrient uptake by the plant. However, some nematodes cause the production of giant or nurse cells whose sole purpose is to feed the nematode (for example, root-knot nematodes). These nematodes not only physically damage a root from their activities but also redirect plant food for themselves.

Foliar Damage Symptoms Water and Nutrient Stress – Premature Wilting Leaf Yellowing (Chlorosis) Plant Stunting Irregular Symptom Patterns Foliar Symptoms - Damage from nematodes in plant foliage may be manifest directly from feeding activity on leaves, flowers and stems. Foliar feeding nematodes, however, are much less prevalent than those feeding on roots. Root feeding nematodes produce foliar symptoms that mirror root damage. In fact, most foliar-induced symptoms are the same as those plants show when not receiving sufficient water and nutrients – wilting, yellowing, and stunting. As a result, nematode problems are often misdiagnosed and blamed on a lack of fertilizer and water.

Foliar Symptoms- Aerial View Aerial Photo -The sugarbeet field is almost entirely affected by sugar beet cyst nematodes. The field shown at the top was treated with a chemical (called nematicide) to reduce damage from the cyst nematodes. Note the dark green nematicide-treated strips in the field at the bottom of the photo.

Foliar Symptoms – Oval Pattern Damage Patterns – Unlike the previous slide, most nematode damage will result in stunted, yellowing or both symptoms on plants. Areas of damage in a field are spotty across a field and irregular, usually oval, in shape. Nematodes almost never produce ‘row’ patterns.

Foliar Symptoms- Plant Death Plant Death – These grape tomatoes are in the last stages of decline/death due to root-knot nematodes. Nematodes do not usually kill plants outright but rather lead to a slow decline sometimes leading to death.

Foliar Symptoms- Stunting Stunting – Cabbage plants in rows shown in this slide are the same age and planted on the same day. A nematicide was used to kill ‘sting’ nematodes before planting the cabbage on the left.

Foliar Symptoms- Leaf Yellowing

Foliar Symptoms- Stunting Stunting – The cabbage plant on the left simply looks young, not necessarily nematode damaged. However, it is greatly stunted compared to the same age plant on the right.

Foliar Symptoms- Slow Decline Slow Decline – Florida citrus is greatly affected by three different nematodes – ‘citrus, burrowing, and lesion’. Burrowing nematode damage shown here results in citrus ‘slow decline’ disease, note spare vegetation on tree in the foreground. Trees gradually produce less fruit, leaves and new growth. Whole orchards have been destroyed by this nematode

Foliar Symptoms- Toppling Toppling Disease – ‘Burrowing’ nematodes cause damage to banana roots and banana yield is affected. However, the major problem caused by nematodes on this plant is ‘toppling’. Banana roots are so severely affected that they cannot hold the tree upright once the extra weight of the developing fruit is added.

Root Damage Symptoms Galled Roots Stunted Roots Swollen Root Tips Root Lesions Increase in Lateral Roots Root Damage Symptoms – Nematode damage on roots is only readily diagnosed in a few cases. For example, presence of root swellings or galls would usually indicate that root-knot nematodes are present. Also, plant root systems that show stubby and swollen root tips are typical of sting and stubby root nematode damage. However, most nematode damage simply results in stunted root systems or roots that show areas of dead tissue (lesions). These symptoms could be caused by a variety of other causal agents. For accurate problem determination, nematodes must be extracted and identified in a laboratory. Slide 22. Root Damage Symptoms – Nematode damage on roots is only readily diagnosed in a few cases. For example, presence of root swellings or galls would usually indicate that root-knot nematodes are present. Also, plant root systems that show stubby and swollen root tips are typical of sting and stubby root nematode damage. However, most nematode damage simply results in stunted root systems or roots that show areas of dead tissue (lesions). These symptoms could be caused by a variety of other causal agents. For accurate problem determination, nematodes must be extracted and identified in a laboratory. Slide 23. Root Galling – Root-knot nematodes are widely distributed and major soil pests worldwide. These nematodes cause plant cells to multiply rapid producing ‘knot’ (galls) on roots. Females are imbedded inside these galls. As indicated, root galling is easily observed and quite diagnostic for presence of these nematodes.

Root Symptoms- Galling Root Galling – Root-knot nematodes are widely distributed and major soil pests worldwide. These nematodes cause plant cells to multiply rapidly producing ‘knots’ (galls) on roots. Females are imbedded inside these galls. As indicated, root galling is easily observed and quite diagnostic for presence of these nematodes.

Root Symptoms- Cyst Nematodes on Roots Cysts on Roots – Cyst nematodes do not cause major malformations or lesions on roots. However, their swollen bodies are on the outside the root. By careful examination with a magnifying glass, ‘pearly’ white cysts on the roots can be seen.

Root Symptoms- Peanut Pod Galling The peanut root-knot nematode is the most damaging nematode pest on the peanut crop. The nematode affects peanuts in a number of ways including reducing plant growth, hence pod development. Additionally however, the nematode may cause pod abortion, weaken pegs so that they remain in the ground, open wounds for rot organisms, and generally reduce nut quality.

Root Symptoms- Lesions Root Lesion - Root lesions may be caused by any number of factors. Among these are nematodes, primarily lesion and burrowing, that produce dead areas on roots. For accurate diagnosis, however, soil and root samples must be analyzed in a laboratory.

Root Symptoms – Sweet Potatoes Sweet Potatoes - Nematodes not only damage roots, thus affecting plant growth, but also other plant parts present in soil. Root and tuber crops are affected in appearance and quality as well as quantity produced. Pictured here are sweet potatoes infected with root-knot nematodes resulting in a serious reduction in both appearance and quality.

Root Symptoms - Irish Potatoes Irish Potatoes - Root-knot nematode damage in Irish potatoes is a major problem in production of this crop. The stained dark red spots pictured here are females of the root-knot nematodes. Potatoes affected by nematodes will rot in storage.

Root Symptoms- Potato Rot Nematode Potato Rot - The ‘potato rot’ nematode causes accelerated tuber rotting as shown in this photograph. Tubers infected with these nematodes are a total loss

Root Symptoms- Sprangling Root Sprangling - Nematodes are a major problem on some root crops, reducing yield and resulting in rotting but sometimes more importantly, growth distortion. For example, even low populations of nematodes can cause root ‘sprangling’ on crops such as carrots and turnips, thus rendering them unmarketable.

Disease Interactions Nematodes cause plant disease and can make fungal and bacterial diseases worse. Disease Interactions - Nematodes not only cause plant disease by themselves but also increase plant damage caused by other disease-causing organisms such as bacteria and fungi. For example, the presence of nematodes provides entry points for invasion of Fusarium wilt fungi in a number of crops. (Note in the photograph that presence of the Fusarium wilt fungus showed little affect on plant growth, but damage dramatically increased in the presence of root-knot nematodes (Mi, Mh, and Mj). Control Fusarium(F) Mi +(F) Mh +(F) Mj +(F) An example is Fusarium wilt where root-knot nematodes create entry points for the fungus.

Problem Identification Combinations of: Foliar Symptoms Roots Symptoms Cropping History Laboratory Analysis Problem Identification – To identify a nematode problem, one must consider individual plant foliar and root symptoms, field damage patterns, plus have an idea of cropping history (were susceptible crops previously grown?). If nematodes are suspected, a final laboratory analysis is often needed to confirm suspicions.

Sampling Basics County Agents have kits available Sample 10”-12” deep; in turf 4”-6” Sample only in moist soils – Not dry or wet Use a plastic bag only Do not let the sample get too hot or cold Send 1 pint of soil and 1 cup of roots Send for extraction ASAP Do not allow samples to become hot or frozen, either way nematodes will be killed Sampling – Proper sampling and handling of nematode samples are a must or laboratory analyses will not provide accurate results. Carefully follow the dos and don’ts listed on the slide for accurate laboratory results. Remember, nematodes are living animals and will die/disappear from samples if not handled properly.

Management Methods Exclusion Sanitation Rotation Plant Resistance Fallow Solarization Nematicides Management - Methods for nematode management are generally broken down into: 1) exclusion, 2) sanitation, 3) cultural practices, 4) plant resistance, and 5) nematicides. The heading, cultural practices, is not listed in the slide. Rather, those cultural practices of rotation, solarization, and fallow are listed separately. This was done to emphasize the importance of these techniques, particularly where use of nematicides are prohibited or not available.

Exclusion/Sanitation Buy or grow transplants that are nematode-free. Use nematode-free soil or potting medium Clean tools and equipment when changing areas or fields Remove infected plant roots Exclusion/Sanitation – Keep pests out!! For example, buy or grow transplants that are nematode-free. The soil medium is obviously the greatest consideration here and it should be nematode-free. Remove potentially contaminated soil and plant materials from tools and other equipment when moving from one area or field to another. For nematodes, this is usually just a matter of rinsing tools thoroughly with water.

Rotation Move garden to a new location Rotate grasses with broadleaf plants Plant cover crops that are poor hosts Keep weeds in check, many are hosts Maintain high organic matter levels Irrigate frequently and use higher fertilizer rates Rotation – This ‘cultural practice’ can/should be a cornerstone of any nematode management program. In most annual crops, proper crop rotation with non- or poor hosts of nematodes is the only nematode management needed. However, economics of growing ‘rotation’ crops, practicality including land requirements, and specific nematode host range many times limits rotation options. This practice should always be keep in mind, even in small garden plots, where perhaps sweet corn could be rotated with more susceptible crops such as okra.

Soybean Rotation Soybean Rotation – Planting a poor or nonhost of nematodes for two years will generally reduce nematode populations and allow acceptable plant growth of a susceptible crop.

Resistance Resistance breeding has been mainly to root-knot nematode (Meloidogyne spp.) Resistance, however, may be to only 1 root-knot species Examples of resistance can be found in tomato, snap bean and some southern peas Little resistance is available to other nematode species Resistance - The use of plant resistance, when available, should always be encouraged. Resistance to root-knot nematodes is available in crops such tomato, soybean, snap bean, southern peas and several other crops. A word of caution, do not rely solely on plant resistance since certain populations of nematodes can overcome resistance beginning either immediately or sometimes several years after regularly planting the resistant plant.

Resistant/Not Resistant Resistant/Not Resistant – The process of finding, breeding and selecting plants with resistance to nematodes is long and tedious. The plant on the left shows good resistance to root-knot nematodes as evidenced by lack of galling, note the susceptible, galled root system on the right.

Solarization Only works moderately well with nematodes Has added advantage of reducing weed problems Use clear plastic, make sure soil is tilled and moist Use in the hottest months and leave 6-8 weeks Solarization – This practice dramatically increases soil temperatures which in turn kills many weed, fungal, insect and nematode pests. Temperatures that kill nematodes are reached only in the first six inches or so of soil leaving living nematodes present at lower depths. Thus, correct use of solarization will reduce nematode populations, but not enough to prevent all nematode damage to crop plants. It is only useful to minimize nematode damage but should be used in combination with other management practices.

Solarization- Laying Clear Plastic Laying Clear Plastic – Solarization increases soil temperatures and these temperatures kill nematodes. l Soil temperatures that kill nematodes, however, are only reached to depths of 6-8 inches. Remaining nematodes below this depth are usually present in high enough numbers to still cause plant damage.

Successful Nematode Control Management Summary No single practice will control nematodes, so two or more control methods must be used. Sanitation Successful Nematode Control Management Summary - At least two management practices must be used to minimize nematode damage. In addition, good crop husbandry practices such as addition of organic matter, good soil fertility and irrigation will also help reduce nematode damage. Resistance Chemicals

FAQ - Organic Matter Does compost and organic matter control nematodes? The answer is generally no, however, they increase water and nutrients available to the plant. Thus a healthier plant can tolerate more nematode damage.

FAQ - Resistance My nematode ‘resistant’ plant still had lots of nematode damage? A resistant plant is ‘resistant’ to only a nematode to which it was bred For example, a plant may be resistant to only one type (species) of nematode but not others

FAQ – Wet or Dry Do nematodes cause damage under both wet and dry conditions? Greatest damage is caused when conditions are dry. Wet conditions mask some damage until root rotting from nematode damage begins.

FAQ - Nematicides What is the best ‘nematicide’ available for nematodes? All effective nematicides are restricted use chemicals and cannot be bought without a pesticide license Products found in garden stores are ‘at best’ nematode suppressants. Generally, these products are not recommended for nematode control

FAQ - Fallow cannot feed, they will starve, however: Is fallow recommended for nematode management? Fallow makes sense because, if nematodes cannot feed, they will starve, however: Many weeds are host to nematodes, thus they must not be allowed to grow. At least one growing season of fallow must be used and fallow depletes soil organic matter During the ‘winter’, most nematodes are relatively dormant and do not feed anyway.

UF/IFAS EDIS Publications http://edis.ifas.ufl.edu/TOPIC_Nematodes General Nematology Nematodes in the Yard Lawn Pest Nematodes Landscape Nematodes Urban Tree Pest Nematodes Vegetable Nematodes Fruit Pest Nematodes EDIS Publications - More information on nematode biology, sampling, and management can be found on the UF/IFAS EDIS Website address listed on the slide. EDIS also contains a large amount of information on other plant pests.

Authors: Jimmy Rich and Stanley Hendley; for comment or information, please contact jrich@ifas.ufl.edu Photo Credits: R. P. Esser, R. S. Hussey, W. F. Mai, R. A. Motsinger, A. W. Johnson, D. W. Dickson, A. Steele, H. L. Rhoades, M. A. McClure, J.D. Eisenback, K. R. Barker Entomology and Nematology Department Copyright University of Florida 2003