Leaves^}, remain* short and/ thicken atf the base!

I ^ i

develo p o n

s

Larvae^ v leav e heavil y infected\ % V bulb s

Stem and Bulb Nematode 539

and produce the preadult or infective larva. T h e latter can withstand adverse conditions of freezing and of extreme drying for long periods in fragments of plant tissue, stems, leaves, bulbs, s e e ds or in the soil.

Under favorable moisture and temperature conditions the preadult larvae b e c o me active. Whe n the aboveground parts of host plants are covered with a film of moisture the nematodes travel upward to the ne w leaves and shoots, which they penetrate through the stomata, through cracks, or directly at the b a se of stems or in leaf axils. After entering the host they pass through the fourth molt and b e c o me males and females. T h e females then lay e g g s, mostly after fertilization by the males. A complete cycle from e g g to e g g usually lasts about 19-25 days. Reproduction takes place in succulent, rapidly growing tissues or in storage organs and continues throughout the year, although it is retarded or s t o p p ed by low temperatures. Ditylenchus dipsaci is an internal parasite of bulbs, stems, and leaves and passes generation af-ter generation in these tissues e s c a p i ng to the soil only when living conditions in the plant tissues b e c o me unfavorable. Whe n heavily infected bulbs decay, preadult larvae pass out and sometimes accumu-late about the basal paccumu-lates of dried bulbs as grayish-white, cottony masses, called nematode " w o o l ," where they can remain alive for years.

Development of Disease

Whe n nematodes attack a germinating s e ed or young seedlings, they enter near the root cap of the hypocotyl or at points still within the seed. T h e nematodes remain mostly intercellular, feeding on the parenchymatous cells of the cortex. Cells near the heads of the nema-todes appear to have lost all or a portion of their contents, while cells surrounding these begin to divide and enlarge, resulting in develop-men t of swellings on the seedlings. D e p e n d i ng on the size and con-centration of the swellings the s e e d l i ng may b e c o me malformed, twisted, arched, or otherwise distorted. Splitting of the epidermis of-ten follows the enlargement and opens the way to secondary invaders, such as bacteria and fungi.

In older seedlings or young plants derived from bulbs, nematodes enter the leaves through stomata or penetrate directly through the epidermis in leaf b a s es (Fig. 127). Cell enlargement, disappearance of chloroplasts, and an increase of intercellular spaces in parenchyma tissue follow penetration. T h e se effects often p r e c e de direct contact of nematodes with the cells, suggesting that salivary secretions diffuse in advance of the nematodes. T h e nematodes usually remain and

repro-duce in the intercellular spaces feeding on the nearby parenchyma cells whose contents they c o n s u me without causing appreciable dis-coloration on the cell remains. As the bulbs enlarge the nematodes s e em to migrate down from the leaves either intercellularly or by trav-eling on the surface of the leaves and entering again at the outer sheaths of the stem or neck, through which they infect the outer scales of the bulbs. Heavily infected stems b e c o me soft and puffy d ue to the formation of large cavities through the breakdown of the middle la-mella and of the cells the nematodes fee d on. Such stems can no longer remain rigid under the weight of the foliage and they fre-quently collapse. T h e nematodes continue their progress intercellu-larly through the outer scales of the bulbs by breaking down the par-enchymatous tissue through the enzymatic action of their salivary secretion. Parenchyma cells are separated from each other and from the vessels, the latter giving a lacy appearance to the scale. T h e mac-erated parenchyma cells have a white mealy texture at first, but sec-ondary invaders usually set in and cause them to turn brown. In early stages of infection the nematodes remain within individual scales, and in sections the infection appears as complete or incomplete rings of frosty white or brownish tissue. In later stages of infection the nema-todes pass from one scale to the next, and thus more scales may b e involved in one ring. T h e spread of the infection within a b u lb contin-ues in the field and in storage until, usually, the entire b u lb b e c o m es affected.

Control

Populations of Ditylenchus dipsaci parasitic on certain crops can b e r e d u c ed by long (two to three years at least) rotations with resistant crops, such as spinach, carrots, potatoes, lettuce. Since this nematode also overwinters in infected bulbs and s e e d s, the n e e d for use of nematode-free sets or seeds is obvious. Infested s e e ds or bulbs can b e disinfested by treating them in hot water for an hour at 46°C. Onion s e ed can also b e freed from nematodes by enclosing it with methyl bromide gas for 24 hours at 24°C in a gas-tight container, and flower bulbs can b e successfully disinfested by placing them in 0 . 5 % formal-d e h y formal-de solution at 43°C for 4 hours.

Small outdoors areas and greenhouse soil can best b e disinfested by steam sterilization of the soil. G o od control of this nematode in large fields can b e achieved by fall fumigation of the soil with the nemato-cides D D, Vidden D, or T e l o ne at 50 gallons per acre. F a rm equip-men t should b e thoroughly steamed or decontaminated before it is brought into the field if reinfestation of treated fields is to b e avoided.

Foliar (Chrysanthemum) Nematode

S e l e c t ed References

C h i t w o o d, B. G., A. G. N e w h a l l, a n d R. L. C l e m e n t. 1940. O n i on b l o at or e e l w o r m r o t, a d i s e a se c a u s ed b y the b u lb or s t em n e m a t o d e, Ditylenchus dipsaci (Kuhn) Filipjev.

Proc. Helminthol. Soc. Wash. 7: 4 4 - 5 1 .

Krusberg, L. R. 1961 . S t u d i es on the culturing a nd parasitism of plant-parasitic n e m a-todes, in particular Ditylenchus dipsaci a nd Aphelenchus ritzemabosi on alfalfa tis-sues. Nematologica 6: 181-200.

N e w h a l l, A. G. 1943. P a t h o g e n e s is of Ditylenchus dipsaci in s e e d l i n gs of Allium cepa.

Phytopathology 33: 6 1 - 6 9.

N e w h a l l, A. G., a nd B. G. C h i t w o o d. 1940. O n i on e e l w o rm rot or bloat c a u s ed b y the stem or b u lb n e m a t o d e, Ditylenchus dipsaci. Phytopathology 30: 3 9 0 - 4 0 0 .

Sayre, R. M., a nd W. B. Mountain. 1962. T h e b u lb a nd s t em n e m a t o de (Ditylenchus dipsaci) on onion in S o u t h w e s t e rn Ontario. Phytopathology 52: 5 1 0 - 5 1 6 .

Southey, J. F. 1965. T h e i n c i d e n ce a nd location of s t em e e l w o r ms on onion s e e d. Plant Pathol. 14: 5 5 - 5 9 .

Yuksel, H. 1960. Observations on the life cycle of Ditylenchus dipsaci on onion s e e d-lings. Nematologica 5: 2 8 9 - 2 9 6 .

Foliar (Chrysanthemum) N e m a t o de Occurrence and Importance

T h e foliar nematode of chrysanthemums, also known as chrysanthe-m uchrysanthe-m eelworchrysanthe-m, is known to b e w i d e s p r e ad in the United States and in E u r o p e. It results in fairly severe losses to the chrysanthemum grow-ers by causing stunting and distortion of plants arising from infested b u d s, and defoliation, dwarfing, or death of shoots infected during the growing season. In addition to chrysanthemum, the foliar nematode or closely related species attack several other plants including aster, dahlia, delphinium, phlox, zinnia, and sometimes tobacco and strawberry.

Symptoms

Affected b u ds or growing points of stems, arising from stolons dur-ing early sprdur-ing, produce short and often abnormally bushy-lookdur-ing plants with short internodes. T h e growing point may b e so d a m a g ed that the shoot does not grow and turns brown. T h e leaves produced from infested b u ds are small and distorted. T h e stem and petioles show brown scars c a u s ed by nematodes feeding externally on these tissues while still in the bud. Shoots so infested seldom d e v e l op into

541

normal plants. Uninfested shoots may exist on the same stool with in-fested ones and they d e v e l op into normal ne w plants. As the season progresses, however, nematodes climb up the stem and attack first the lower and then the upper leaves on which they cause small yellowish spots later turning brownish black. T h e se spots soon coalesce and form large blotches which at first are contained b e t w e en the larger leaf veins (Fig. 128). Eventually the entire leaf is covered with spots or blotches, and it soon shrinks, b e c o m es brittle, and falls to the ground. Defoliation, like infection, progresses from the lower to the upper leaves. T h e nematodes also infest the ray flowers and prevent their development. Severely infested plants die without producing much normal foliage or marketable flowers.

The Pathogen: Aphelenchoides ritzema-bosi

It is a long, rather slender nematode. T h e female measures 0.77-1.20 m m long by about 20 μ in diameter, and the male 0.71-0.93 m m long by 19-23 μ in diameter. T h e y have a prominent caplike lip region and a spear about 12 μ long, with distinct knobs (Fig. 129).

Aphelenchoides ritzema-bosi may live its entire life inside leaves or at the surface of other plant organs. T h e female adult lays its eggs in the intercellular spaces of leaves. T h e eggs hatch and produce the 4 larval stages, and finally adults, all inside the leaf. Whe n leaves b e -come wet the adults leave the infected area and penetrate the s a me or adjacent leaves in which the female, with or without fertilization, lays its eggs. T h e life cycle is completed in about 2 weeks. T h e se nema-todes do not have to s p e nd any part of their lives in the soil but are frequently found there carried by infected, d e ad leaves fallen to the ground, or w a s h ed down by rain or irrigation water when they h a p p en to b e on the surface of plant tissues. T h e se nematodes overwinter as adults in d e ad leaves or b e t w e en the scales of b u ds of infected tissues.

Development of Disease

N e m a t o d es overwintering b e t w e en the b ud scales of basal lateral b u ds or of the growing point of shoots b e c o me activated in the spring and fee d ectoparasitically, by inserting their stylets into the epidermal cells of the tissues or organs in their vicinity. T h u s, stem areas near infested b u ds and the petioles and leaves derived from such b u ds show brown scars consisting of groups of cells killed by the nema-todes. In addition to direct killing of cells the nematodes, through their secretions, affect the physiology of the tissues on which they

Foliar (Chrysanthemum) Nematode 543

F i g. 128. D i s c o l o r ed areas on c h r y s a n t h e m um l e a v es c a u s ed by the foliar n e m a t o de Aphelenchoides ritzema-hosi. (Photo by courtesy of the D e p a r t m e nt of Plant Path-ology, Cornell University.)

fee d and of the whole plant. T h u s they c a u se shortening of the inter-nodes, which results in a b u s hy a p p e a r a n ce of the plant, and also browning and failure of the shoot to grow (blindness), production of low, premature side-shoots, and d e v e l o p m e nt of distorted leaves.

N e m a t o d es infest new, healthy plants by s w i m m i ng up the stem w h en it is covered with a film of water during rainy or h u m id weather.

Whe n they reach the leaves, the nematodes enter through the stomata;

if the leaves are young the nematodes s e em to b e confined to the sub-stomatal cavity for a while, spreading into the mesophyll and the pali-sade layer later on (Fig. 129). T h e p r e s e n ce of nematodes b e t w e en the leaf cells causes no apparent symptoms at first. Soon, however, patches of an o p a q ue brown substance appear within the cells near the nematodes. As the browning in these cells b e c o m es more abun-dant, the number of chloroplasts is r e d u c ed and more cells b e g in to turn brown. By the time the browning reaches the epidermal cells,

Fig. 129. Disease cycle of the foliar (chrysanthemum) nematode Aphelenchoides ritzema-bosi.