Hawaii Institute of Tropical Agriculture and Human Resources College of Tropical Agriculture and Human Resources, University of Hawaii INFORMATION TEXT SERIES 020

Burrouuing Nematodes: fl Menace To Hauuaii Nurseries

O. V. Holtzmann, A. P. Martinez and W. J. Apt NOTE: As part of a structural reorganization, the Hawaii Cooperative Extension Service and the Hawaii Agricultural Experiment Station have been merged administratively under the name HAW AII INSTITUTE OF TRO PICAL A G RIC U L­ TURE AN D HUM AN RESOURCES, College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.

Issued in furtherance of Cooperative Extension work. Acts of May 8 and June 30, 1914, in cooperation with the U.S. De­ partment of Agriculture. Noel P. Kefford, Director and Dean, Cooperative Extension Service, College of Tropical Agricul­ ture and Human Resources, University of Hawaii at Manoa, Honolulu, Hawaii 96822. An Equal Opportunity Employer providing programs and services to the citizens of Hawaii without regard to race, color, national origin or sex. INFORMATION TEXT SERIES 020-05/84 (700) THE AUTHORS

Oliver V. Hotlzmann is a Professor in Pathology, College of Tropical Agriculture and Human Re­ sources, University of Hawaii. Albert P. Martinez is a Specialist in Plant Pathology, College of Tropical Agriculture and Human Re­ sources, University of Hawaii. Walter J. Apt is a Professor in Plant Pathology, College of Tropical Agriculture and Human Resources, University of Hawaii. BURROWING NEMATODES: A MENACE TO HAWAII NURSERIES

O. V. Holtzmann, A. P. Martinez and W. J. Apt

The burrowing nematode (BN) (Radopholus slmlI Is) Is without a doubt the most serious, Individual pest with which growers of export ornamentals have to contend. Its presence In a nursery may mean either the rejection and destruction of a valuable consignment of to the Mainland and/or the expensive and laborious process of trying to locate the source of contamination In the nursery. The subsequent eradication of Infected plants and the disinfestation of the area Is not easily accomplished. The best way to avoid a BN problem Is startin g clean and staying clean. Of course th is Is so easy to say and so hard to accomplish. The pitfalls for contamination of a nursery with BN are many, so the location of the problem area Is often very difficult to accomplish. In order to have control of nursery sanitation one must know the possible sources of BN contamination and those Improper cultural practices which could aid in the spread of the contamination within the nursery once established.

Burrowing nematodes are already recognized a major problem in Hawaii's banana and anthurium Industries and to a much lesser extent In commercial edible ginger.

SOURCES OF BURROWING NEMATODE CONTAMINATION:

The ways that nematodes can enter a nursery are many and often their entry Is peculiar to the specific oprations of a given nursery, some of the ways that nematodes Infest a nursery site are:

1. infecting plants on the site before the nursery was establI shed;

2. brought In with Infected or Infested plants;

3. brought In with contaminated planting media.

Hapu from hawallan tree ferns used In potting media Is suspected of being a source of the BN. However, hawailan tree ferns are not known to be host for the BN. Therefore If the BN is coming In with hapu It Is the result of the harvest of other BN hosts along with the tree fern or from the logs coming In contact of Infested soil during the harvesting operation. A less probable source Is cinder contamination from Infected plants growing In or near the cinder mines.

Page 1 4. Contaminated vegetative seed pieces, pots, or wood previously used for benches or other nursery operations.

5. Contaminated water from open Irriga tio n ditches which receive run-off water from fie ld s or native areas (city water Is free of plant pa rasitic nematodes). Surface run-off water from surrounding areas.

6. Soil movement of any kind, whether for potting mix, landscaping or landfilling. Nematodes also can enter In soil and mud on shoes, hands, and clothes of nursery workers and visitors. Yes, they even enter on the paws and fur of dogs and cats (entry by birds and Insects are more Improbable). Mud and soil on treads of equipment tire s, on equipment accessories, on hand tools used outside.

7. Plants In and around the nursery such as bedding stock plants, landscape plants, native (herbaceous or woody), and adjacent cultivated or weed hosts are suspect.

Burrowing nematodes may be found In most areas where bananas and wild gingers grow. They have been recovered from Infected banana plants In the remote Hanakaplal and Hanakoa valleys of Kauai, the east slopes of Haleakala on Maul and from run-off water from non-cultlvated areas above Walmanalo on Oahu. The nematode Is e asily Introduced Into new areas with Infected plant material. Subsequently It is disseminated In that area by surface run-off water, wild animals, and any other agent which can move plants or so il. By Itse lf, the nematode being less than a millimeter In length, moves relatively very short distances In Its life span of about a year. Since then the BN spread has been facilitated by various agents e.g. wild pigs and plant collectors of various kinds.

Always be wary of "free" or purchased plants.

Page 2 TYPES OF PLANT INJURY CAUSED BY BURROWING NEMATODES:

Above-ground Symptoms: Above-ground symptoms of plants heavily Infected by BN are similar to those associated with general nutrient deficiency and chronic water stress. The appearance of the plant Is generally unthrifty, with some chlorosis, stunting and wilting at peak transplratlonal times of the day. Generally, environmental stress Is required for the symptoms to show, in fact, the greater the environmental stress, the more pronounced the symptoms. Therefore, one should not expect to see above-ground symptoms In potted ornamentals in the nursery caused by BN since normal cultural care should be adequate to minimize environmental stress. The BN does not enter above-ground parts.

Below-ground Symptoms: Below-ground parts i.e., roots, rhizomes, corms and tubers may be Infected. The most Important effect in most plants Is the destruction of the feeder root system. Weakening of plant support occurs when fleshy root Is invaded and subsequently the nematode colonization of the root causes lesions to form which later rot and enlarge thus g ird lin g and weakening the root system. Sunken lesions may be seen in some corms and rhizomes. In general, root symptoms are not specific for the BN and may resemble those caused by root-rotting fungi. Since the nematode, feeding Internally In the root provide a wound, this area may be Invaded by other root parasites such as fungi and bacteria, some of which need a wound to enter. Thus the BN can either predispose plants to root rotting fungi or intensify existing root rots.

LIFE CYCLE OF THE BURROWING NEMATODE:

The BN is an obligate parasite, I.e., It requires a living host on which it can feed or It may die In 4-6 months. The adult female nematode Is approximately 0.75 mm long. The life cycle, from egg to egg can be completed In about 3 weeks, depending on an available host and favorable environment. Initially, a larval or adult nematode punctures tender root cells In the vicinity of the root hairs, near the tip of the roots. Puncturing and feeding In root cells Is accomplished by a hollow style t in Its head region. Hardened or corky roots are not invaded. The burrowing nematode gets its name from its habit of feeding in the fleshy cortical region of the root and migrating through the tissue. Lesions occur because as the female migrates she may deposit eggs along the way which hatch In 3-7 days. The larval nematodes go through several molts to become an adult and the life cycle process is repeated, thus the root becomes colonized and the breakdown of the root tissue Is first observed as tiny lineal lesions. These enlarge and coalesce with others to form cankers. Larval and adult nematodes may leave the root and migrate to other feeding sites. Identification of BN root lesions may require up to 9 days Incubation and/or examination with microscopes at 30-45x. Positive Identification of the BN may require an adult male or female at magnifications of up to lOOOx.

Page 3 The BN has a wide host range, however, certain Identity Is complicated because of the existence of at least two races, the "banana race" and the "c itru s race", which are Indistinguishable by a microscope. The "citrus race" attacks both citrus and bananas and many other hosts, while the "banana race" Infects bananas and a number of other hosts, but not citrus. The host range of the "banana race" Is more restricted than that of the "citrus race". Spreading decline of citrus, caused by the "citrus race" Is one of the most Important diseases of c itru s In Florida, but has not as yet been found In California, or any of the Pacific Islands. Because of this Inability to readily distinguish between the two races, California has Imposed the very rigid quarantine restriction on a I I forms of R. slmlI Is. the Burrowing Nematode. Over 300 hosts of BN without regard to race have been reported worldwide. It has been recently reported that a population of BN Infecting Anthurlum from Hawaii was able to Infect Citrus aurantlcum (sour orange) In Florida and that the mating behavior of the Florida citrus race and the Hawaiian Anthurlum population was similar. Studies to confirm this work are currently underway.

The following three tables contain names of species of plants which have been reported as hosts of jL. sIm11 Is and Radopholus spp. In Hawaii and other Islands of the Pacific. These species of plants are found in 41 fam ilies of plants. Families which have 5 or more reported host species are Araceae, Gramineae, Leguminoseae, Marantaceae, Musaceae, and ZINGIBERACEAE. ALL THE REMAINING FAMILIES have from one to three species of hosts of the BN.

The BN Is a very formidable foe because of Its small size and wide host range. Other Important features which make It so d iffic u lt to eradicate Is Its ability to live within roots, migratory habit, and ease at which It can be dispersed from one area to another by the aid of outside agents.

SOME METHODS FOR NEMATODE CONTROL IN NURSERIES:

The key to nematode control in ornamental plants Is to sta rt with nematode-free plants In an area free from nematodes. Subsequently every effort should be made to avoid the entrance of the nematodes Into the nursery operation. All of the Items covered In Table I, "A Checklist for Nursery Sanitation" must be followed at all times.

The approach to nematode control w ill depend upon the type of operation e.g., certified nursery for export, nursery for sale of local landscape plants, or growing plants for cut-flower production. It should be obvious that the approach to sanitation Is generally much more strict In the certified nurseries than In nurseries for local sale and less In nurseries for the production of cut-flowers. However, In all cases it Is still Important to start with nematode-free plants and plant them in media or soil that Is known to be free of nematode pests.

Page 4 1. Nursery establishment — Know the agricultural history of the site on which the nursery will be established. If the site Is suspected of being Infested with nematodes, soil sampling and laboratory analysis as prescribed by a county agent should be followed. If the area is Infested, fumigation of the entire area with methyl bromide should be made. Knowledge of the lim itations of fumigation Is a must, as failure to take into account such limitations w ill result in a waste of time and money. Fumigants w ill not penetrate undecomposed roots and other plant material nor will lumps of compacted soil be penetrated. The fumigant gas will not penetrate the soil much further than the depth it is t ille d nor w ill wet s o ils be penetrated. On the other hand, fumigation of aa lava soils is Impractical because there Is no Impervious sub-soil to retain the gas for a period of time sufficient to kill the nematodes.

2. Clean Planting Material — The most satisfactory method of ridding Infected plant parts of nematodes is hot water. However, there are definite advantages as well as disadvantages to hot-water treatment. The advantages are: I) many pathogens inside the plant are killed; li) relatively easily accomplished and Inexpensive. Disadvantages are: I) plant tissue may be Injured; ii) plants vary in their tolerance of heat both In species and stage of growth or development; I I I ) plants are less heat-sensitive In a dormant stage, however, some plants do not have a well defined dormant stage; Iv) heat breaks dormance so plants (rhizomes, etc.) must be planted quite soon after treatment. Not all plants or plant parts tolerate a heat treatment.

The common treatment for bare-rooted nursery stock and some other plant materials Is 50°C (121.5°F) for 10 minutes. Modifications of temperature and time are necessary for some plant material but should be first established experimentally.

3. Sol I and Med I a Treatment — Steam or a mixture of steam and gas are some of the more common methods of ridding soil or planting media of nematodes. These Involve two types:

Sol I SterI IIzatlon: raising the temperature to 82°C (180°F) and held there for 1/2 hour. This treatment kills all organisms and weed seeds. In treatment of soil two problems may arise, I.e., I) because the soluble salt content of the soil increases, Injury to seedlings may occur If transplanted In treated soil too quickly (wait about two weeks) and Ii) toxic concentrations of specific elements, e.g., manganese may be released.

Sol I Pasteurization: is accomplished by treatment of soil with low pressure stem, electric coils, etc. Soil Is held at 60-71 °C (140-160°F) for 1/2 hour. At this rate all plant disease agents are k ille d as well as most germinating seeds. The d iffic u ltie s noted for steam sterilization are usually not encountered.

Page 5 Post-PIanting Treatment with Nematic Ides: Several systemic nematicldes e.g. a lllcarb , fenamlphos, oxamyl, etc. have shown promise In the treatment of established plants for the reduction of nematode populations. However, to date no chemical treatment has been demonstrated to tally effective In consistently eradicating plants of nematodes for quarantine purposes. However, because of their partial effectiveness, the application of systemic nematicldes may hamper subsequent efforts to locate the exact areas of nematode contamination In a nursery.

4. Disinfestation of Crates, Flats. Pots, Containers. Benches, etc. Benches, containers crates, flats, post, etc. may be dipped or sprayed to wetness with a 55? solution of a commercial bleach (sodium hypochlorite, 5.255?) or 45? formaldehyde solution. Care should be exercised to make these treatments only in well ventl Mated areas using the proper safety precautions of protective clothing, gloves, foot-wear and suitable respirator. Drift or splashing of these solutions on growing plants may cause Injury.

Page 6 TABLE I. A CHECKLIST FOR NURSERY SANITATION:*

Sol If Containers and Materia Is:

All soil or potting media treated with steam or nematicldes In accordance with recommendations of Hawaii State Department of Agriculture or County Extension Agent.

.Soil storage areas, potting benches, and containers treated with a dlslnfestant.**

.Tools treated with a dlslnfestant** before use In treated soil.

.Benches treated with a dlslnfestant** after each crop Is removed.

.Use only new or clean materials In plant propagation, e.g. air-layer Ing, etc.

.Use a mesh constructed top for raised benches.

P la n ts:

.Stock plants segregated and Isolated from production areas and operations.

.Cuttings taken from only clean stock plants.

.Top cuttings used, at least 12 Inches *rom the soil line.

.Cuttings broken off or knives used which are frequently dlsi nfected.

.Propagation material placed on clean surfaces and protected from contamination before planting.

Sanitary Practices:

.Providing good drainage for nursery site so that water runs away from propagation houses.

.Not using burrowing nematode-susceptible plants for landscaping or locating burrowing nematode suspectlble plants close to propagation houses.

.Not placing plants over plants.

.Clean plants, containers and soil kept apart from untreated plants and materials.

.New planting materials kept Identified and Isolated until determined to be nematode-free by root and soil sampling and laboratory diagnosis.

Page 7 Material suspected of contamination Immediately removed or destroyed and surface areas treated with a dlslnfestant.**

Unnecessary handling of treated soil strictly avoided.

Splashing of water avoided.

Hose nozzles kept off the floor.

Not allowing the placement of Items such as: unsanitized fla ts, pots, and boxes, shoes, boots, etc. on the benches by workers and visitors where clean plants are growing.

Hands washed before handling clean material.

Adapted from: "a checklist for nursery sanitation” NIPM Item #14.2 (Rev. 12/1/78). C alifornia Department of Food and Agriculture, Division of Plant Industry.

D isinfe stan t(s) used must be approved by Hawaii Department of Agriculture, Division of Plant Industry and/or the Cooperative Extension Service. TABLE II. Hosts of the burrowing nematode,Radopholus similis reported in Hawaii.*

HOST ______ISLANDS RECORDED SCIENTIFIC COMMON FROM**

A1 pInI a speclosa shel1 glnger Oa

Ananas comosus pineapple Oa

Annona murica+a soursop Oa

An+hurium andraeanum anthuri urn Ha, X

Cajanus flavus pigeon pea Oa

Canna edu1 Is edible canna Oa

Chrysanthemum frutesens marguerite Oa

Col ocas I a esculenta taro Ka

C. esculenta globullfera dasheen Ka

Cyperus graci1 is McCoy grass Oa

C. papyrus papyrus

C. rotundus nut grass Oa

Hedychlum coronarlum white ginger Oa

H. flavescens yellow ginger Ha,

HelIcon la carlbaea Oa ' yellow'

H. humiIts cv. 'dwarf humi1 I s ' dwarf lo b ste r's claw Oa

H. humi1 Is lobsters claw

H. wagnerana (=H. strlcta ) Peru helI con I a Oa

H. sp. Royal helI conia Oa

H. sp.

Page 9 HOST ISLANDS RECORDED SCIENTIFIC COMMON FROM**

Ipomoea batatas sweet potato Oa

Maranta leuconeura arrowroot

M. leuconeura var. massangeana arrowroot Oa

Maranta sp. Oa

Musa acuminata (AAA) cv. 'dwarf cavendish' Chinese banana Ha, Ka, Ma, Oa

M. a. (AAA) cv. giant Michel bluefleld Ka

M. a. (AAA) cv. Iholena Ka, Oa

M. a. (AAA) cv. I acatan PhilIppine Iacatan Oa

M. acuminata X balblslana (AAB) cv. Mala maoli hal Ka, Oa

M. acuminata X baI bis!ana (AAB) cv. Popoulu moa Ka, Oa

M. acuminata X balblslana (AAB) cv. Popoulu pokole Oa

M. balblslana (BB) Ka, Oa

M. ornata Ka, Oa

M. paradlslca banana Oa

Musa sp. Ma, Oa

Philodendron sp.

Saccharum officinarum sugar cane Ka, Ma, Oa

Page 10 Strelitzla reglnae blrd-of-parad1se Ha, Ka

S+reli+zI a sp.

Zingiber officinale edible ginger Ha, Oa

* From the literature, Plant Disease Clinic records and the personal file s of 0. V. Holtzmann. PDC records were Identified by W. J. Apt and 0. V. Holtzmann.

** Islands of Hawaii: Hawaii (Ha), Kauai (Ka), Maui (Ma), Molokai (Mo) and Oahu (Oa). Lack of record from any one island does not imply the absence of the burrowing nematode from those Islands or hosts thereon.

Page 11 TABLE III. Plants of Hawaii reported as hosts of unidentified species of Radopholus.*

HOST NAME ______ISLANDS RECORDED SCIENTIFIC COMMON FROM**

Allium cepa onion, bulb Ma, Mo

A. fistulosum onion, green Ha

Axonopus a ffin is carpet grass Ha

Bougainv iI lea sp. Oa

Calathea alballneata Oa

C. metallica zebra plant Oa

C. zebrina Zebra plant Oa

Chrysanthemum morifolium f l o r i s t ’s chrysanthemum Ma

ChrysophyI I urn oliviforme satin leaf Oa

Euphorbia pulcherrlma poinsettia Oa

Microsorlum scolopendrta laua'e fern Oa

Musa acuminata (AAA) cv. Cocos dwarf bluefield banana Ma

M. a. (AAA) cv. giant cavendish Williams hybrid Ha, Ma, Mo, Oa

M. a. (AAA) cv. gros michel bluefleld banana Ma, Ka, Oa

M. paradislaca Ma

M. paradislaca var. koae Oa

Musa sp. banana Ha, Mo

Nerium oleander oleander Oa

Persea amerlcana avocado Oa

Petroselinum crI spurn parsley Oa

Phaseolus vulgaris Oa

Pisum sativum, var. macrocarpum Chinese pea Ma

Page 12 HOST NAME ISLANDS RECORDED SCIENTIFIC COMMON FROM**

Poltanthes tuberosa tuberose Oa

Polystlchum adlanti forme leather leaf fern Oa

Scaevola serlcea beach naupaka Oa

Sclndapsus aureus pothos, taro Oa

StrelItzla reglnae blrd-of-paradlse Oa

Strongylodon macrobotrys Jade vine Oa

Vinca major perIwInkle Oa

Zoysla tenuIfolI a Japanese temple grass Oa

* Plants or locations on record at the Plant Disease Clinic In Table I are not repeated.

** Islands of Hawaii: Hawaii (Ha), Kauai (Ka), Maul (Ma), Molokai (Mo) and Oahu (Oa).

Page 13 TABLE IV. Plants of other Pacific islands reported to be hosts of Radopholus sim ilis*

HOST NAME

SCIENTIFIC COMMON PACIFIC ISL/

Alphi+onla zizypholdes to I Tonga

AIpInI a purpurata red ginger F iji

Arachis hypogaea peanut F iji

Axonopus compressus carpet grass, broad 1eaved F iji

CalophyIlum vltiense Tonga

Cocos nuclfera coconut Samoa

Curcuma domestica turmeric F iji

Cyathea sp. tree fern FIJI

DIoscorea a lata yam F iji

D. esculenta lesser yam FIJI

Gmelina arborea gumhar Tonga

Hibiscus esculentus okra FIJI

H. man I hot F iji, Tonga

Man I hot esculenta cassava Samoa

MIscanthus floridulus Island reed grass F IJI, Tonga

MyrIstlca InutiI 1s wild nutmeg Samoa

Nauclea dlderrlchiI opepe Samoa

Pandanus spp. pandanus Tonga

Pinus carlbaea Caribbean pine Fiji

P. el 1lo ttiI slash pine Fiji

P. khasya Tonga

Pi per aduncum Fiji

P. methystlcum awa, kava Fiji

Page 14 Plelogynlum trlmorlense Queensland hog plum Tonga

Polygal a pan Iculata root-beer plant Samoa

Pometla plnnata langslr FIJI

Psldlum guajava guava Fiji

Saccharum edule FIJI asparagus Fiji

Schlzostachyum glauclfollum native bamboo Samoa

Solanum melongena eggplant Samoa

Swletenla macrophylla broad-1 eaves mahogony Fiji

Syzyglum (Eugenia) malacense Malay or mountain apple Fiji

Vtgna sine n sis cowpea FIJI

V. ungulculata cowpea Fiji

* Hosts of Radopholus slmllls of some Pacific Island plants not listed In Table I. Compiled from: Orton Williams, K. J. 1980. Plant parasitic Nematodes of the Pacific. Technical Report, Volume 8, UNDP/FAO-SPEC Survey of Agricultural Pests and Diseases In the South Pacific. 192 p.

Page 15

DISCLAIMER

The use of trade names is for the convenience of readers only and does not constitute an endorsement of these products by the University of Hawaii, the College of Tropical Agriculture and Human Resources, the Hawaii Institute of Tropical Agriculture and Human Resources, the Hawaii Cooperative Extension Service, and their employees. Materials and rates of chemical applications listed herein are based on the latest infor­ mation available at the time this publication went to press. Supplemental information will be disseminated as the need arises and usually will be distributed through the offices of the County Extension Agents. Infor­ mation provided herein is for educational purposes only.