World Dissemination of the Cereal-Cyst ( avenae) and Its Potential as a Pathogen of 1 J. W. MEAGHEW Abslracl: World distribution of the cereal-cyst nematode is herein reviewed. It is suggested that Heterodera ave,me originated in Europe and has been widely disseminated, largely by the activities of Man but also by wind movement of cysts. So far, it may not have spread to some major wheat-growing regions of the New World, but a non-friable soil structure limits popula- tion level and disease. Yield loss could result from the introduction of new cultivars to developing countries where H. avenae has not been detected or where existing cultivars possess tolerance. Key H'ords: wheat, , , , ecology, nematode-fungus interactions, resistance.

Over the last 20 years, there has been distribution of this nematode, its role as a an increased awareness in many countries disease agent, and its potential as a factor regarding the occurrence and economic limiting cereal production, particularly importance of the cereal-cyst nematode wheat. ( Woll.) as a cause of disease in wheat (Triticum aestivum L.). DISTRIBUTION Oats (Avena sativa L.), barley (Hordeum The cereal-cyst nematode was first vulgare L.), and rye (Secale cereale L.) are recognized as a parasite of cereals in also hosts of H. avenae but, although their Germany (29) and is now recorded in most importance is well recognized in some wheat-growing regions of the world (52). regions of the world, the acreage and Recognized for many years as the cause of production o[ wheat exceeds that o[ any yield loss in cereal crops in most European other grain crop. It is the principal food of countries and in the Province of Ontario, about one-third of the world's people and Canada (17, 27), it was known in most of ranks next to rice (Oryza sativa L.) in these countries as the -cyst nematode importance as a food crop. Rice, however, because the greatest effects of disease were is not a host of H. avenae. observed in oats. In recent years, however, My personal knowledge of diseases most attention in Europe has been directed caused by this nematode is based primarily toward control of the disease in barley (9). on Australian experience. Until recently, Heterodera avenae has been described as however, most of the literature on the a parasite of crops grown in the cool- morphology, ecology, symptomology, and temperate zone (16, 24), but it is by no yield loss associated with this nematode means confined to cool temperate regions was based on observations and experiments as it has also been recorded in Italy (40), in Europe and Ontario, Canada. In the Tunisia (11), Spain (56), Portugal (30), last few years, indications o[ some im- Greece (21), Yugoslavia (19), Israel (41), and portant differences have emerged from Australia (10). In India, it is known as the research in other wheat-growing regions. cause of "Molya" disease, an important These differences have provided informa- problem in wheat and barley crops in that tion on the ecology and survival of the country and particularly so in the states of nematode. Increased insight into host- Rajasthan, Haryana, and Punjab (51). This parasite relationships and pathogenesis of nematode species is common in Japan and disease, and information on yield losses and in the USSR as far west as Siberia, but it is economic control measures have resulted not known in China. It was recorded in from experiments in different countries. 1975 in New Zealand (18), but the most Using information obtained from research recent record of major significance is the in both the Old and New World, I will discovery of its presence in a limited area discuss, in this paper, the present world in Washington County, Oregon, U.S.A. (23). Received for publication I March 1976. H. avenae had not previously been recorded 1Symposium paper presented at the joint annual meetings in the U.S.A. and is still unknown in the of the Society of Nematologists, and the American Phyto- pathological Society meetings, Houston, Texas, U.S.A. 10-14 prairie provinces of Canada. August 1975. There is only one record of H. avenae 2Victorian Plant Research Institute, Burnley Gardens, Burnley, 3121, Victoria, Australia. occurring on the South American continent 10 Journal of Nematology, Volume 9, No. 1, January 1977 -at one location in Peru (28), and it has TABLE 1. The occurrence of the cereal-cyst not been recorded in South Africa (van den nematode (Heterodera avenae). Berg, private communication) despite state- ments to the contrary (17, 23, 27). Country Year Reference

DISSEMINATION East Germany 1874 29 Holland 1891 47 Those countries in which H. avenae has Denmark 1897 20 been detected are listed in chronological Sweden 1897 25 order according to the year of record England 1908 55 West Germany 1923 58 (Tahle 1). This list should not be expected U.S.S.R. 1925 15 to provide a clear indication of the nema- Norway 1926 50 tode's origins or its dissemination pattern. Australia 1930 10 Nevertheless, there does appear to be good Canada (Ont.) 1935 45 evidence that H. avenae is indigenous to Scotland 1946 7 Tunisia 1953 11 northern Europe and possibly to Germany Italy 1953 40 where it was originally detected in 1874. Japan 1954 22 If this hypothesis is correct, it would Israel 1956 41 indicate that the original host of H. avenae Belgium 1957 4 Peru 1958 28 is either oats or rye rather than wheat or India 1959 44 barley. Oats and rye are both believed to Poland 1960 59 have had their origins as a cultivated crop France 1961 46 in Europe, whereas wheat and barley Eire 1962 13 originated in Asia Minor and are the oldest Spain 1963 56 Portugal 1963 30 known cultivated plants (3). Northern Ireland 1964 1 If the areas in which H. avenae is known Switzerland 1965 49 to occur are examined (Fig. I), it is evident (; reece 1966 21 that the nematode is widespread in Europe. Yugoslavia 1966 19 With the exception of Israel, however, it Bulgaria 1967 53 Czechoslovakia 1967 26 has not been recorded in countries around U.S.A. 1975 23 Asia Minor or in any of the other ancient N ew Zealand 1975 18 centers of wheat production such as Iraq,

, /

FIG. 1. Areas of wheat production and world occurrence of the cereal-cyst nematode Heterodera avenae White dots show countries or regions where the nematode has been recorded (cf. Table 1). Cereal-Cyst Nematode: Meagher 11

Iran, and Afganistan. This apparent distri- or the movement of water. In Australia, bution may merely reflect the number of however, the rapid dissemination of cysts nematologists in these areas, but evidence appears to have been due largely to move- for a European origin is also supported by ment by wind. In that country, the the presence of a greater number of H. nematode was first described as a parasite avenae biotypes there. In addition, Heter- of cereal crops in South Australia in 1930 odera hordecalis, a cyst-forming species (10). There is no evidence that H. avenae which also attacks cereals, has recently been is indigenous, but herbarium specimens found in northern Europe (2). The ide~lti- show that it has been present since at least fication of five biotypes of H. avenae in 1904 (34). It was probably introduced from India (31), however, suggests that it has Europe in the nineteenth century and it is also been present in that country for many already widespread in the wheat belt of years. southeastern Australia (34). For about 8 The spread of wheat and barley produc- years, H. avenae has also been recognized as tion in the Old World coincides with the a cause of poor growth of wheat near Neolithic Revolution, when Man first began Geraldton, Western Australia. to practice farming, so wheat was intro- It has been shown that cysts of duced to Northern Europe by about 4,000 Heterodera rostochiensis Woll. can be B.C. The dissemination of H. avenae moved by wind over limited distances (57), throughout the Old World would have and eggs in cysts of this species can survive commenced about the same time. long periods of desiccation (43). Until Today, wheat is the most widespread recently, eggs within cysts of H. avenae were cereal crop. It accompanied the Europeans thought to be very sensitive to desiccation, in the course of their overseas expansion but it is now known that eggs within and partly adapted to cold climates mature cysts can survive in air-dry soil for (through vernalization and hardening) and at least 13 months (33), or in a dry atmos- to hot climates (by growth at hi~her phere (75-40% RH) for at least 5.5 years altitudes). The environmental conditions (35, 36). to which wheat has become adapted have The Mallee soils of southeastern Aus- not always been suitable to H. avenae and tralia vary in texture from sands to sandy may be the reason that its distribution in loams. During periods of drought, they are some wheat-growing regions of the New often subject to wind erosion and, in some World is limited; or, it may not have been seasons, violent dust storms develop with introduced at all as wheat has been inten- every strong wind. By means of dust traps, sively cultivated in many of these areas for viable eggs have been recovered from cysts less than 100 years. carried by the wind (35). With the demon- Thus, the known distribution of H. strated capacity of eggs to survive long avenae in the Australian wheat belt and its periods of desiccation and the frequency of recent detection in New Zealand and the dust storms in this area, it is not surprising U.S.A. adds importance to the question of that infestation is widespread, even though dissemination and its potential for future much of the Mallee was only settled in the spread. p:lst 50-60 years.

MEANS OF DISSEMINATION FACTORS LIMITING In the Old World, there is little doubt DISTRIBUTION OF that Man, in his migration and cultiva- THE NEMATODE tion of new land for cereals, was largely Soil: Despite the apparent ease of dis- responsible for the long-distance transport semination of H. avenae by wind or other of cysts--either in soil attached to boots, means, all wheat-growing regions adjacent tools, and equipment, or through his de- to diseased areas may not become infested. liberate movement of soil, alone or with Both distribution of the nematode and plants. Cysts could have been transported symptom expression are clearly influenced in the same way to the New World. by soil type (14, 17, 32, 34). In Victoria, H. Once established within a field, cysts or avenae could only be detected in the sandy, larvae may be disseminated by cultivation solonized, brown soils of the Mallee and the 12 Journal of Nematology, Volume 9, No. 1, January 1977 grey clay, but friable, soils of the Wimmera for at least 1 year when stored dry (75-40% district (32, 34). This nematode species is RH) but rapidly lose viability when stored widespread on similar soils in South Aus- at 21 C under moist conditions (36). Also, tralia and in a limited area of New South few larvae are able to survive in moist soil Wales. These soils are characterized by good for more than 8 weeks at temperatures physical structure. H. avenae has not been above 20 C (Meagher, unpublished data). detected on the heavy, poorly-structured If these results can be extrapolated to field soils in other wheat-growing regions of conditions, they indicate that survival is Victoria which are adjacent and climatically not favored by continually high tempera- similar to the infested areas. tures and moist soil, as are present in There is a consistent association of tropical regions. increased disease severity with lighter soil There may be little requirement for types within infested areas in Victoria (34). the long-term survival of either eggs or This association has also been observed in larvae in soil under certain climatic condi- Canada (45), Europe (27), and India (51). tions and cultural practices. For example, Structural properties of lighter soils (14, 34), maize (Zea mays L.) is an efficient host of which provide good drainage and aeration, H. avenae and, in India, both wheat and appear to favor the maintenance of nema. maize crops are equally attacked when tode populations, perhaps by greater grown in rotation (60). Under these circum- emergence and mobility of larvae or stances, there may be two generations of survival of higher numbers of eggs. How- the nematode per year, but this has not yet ever, in Australia, disease symptoms on the been observed in the field. lighter soils are also intensified by increased leaching of nutrients, particularly nitrogen FACTORS AFFECTING (34). ECONOMIC DAMAGE Climate: Patterns of larval emergence Cyst and larval populations: In Aus- appear to be related to the soil temperatures tralia, the rapid increase in nematode that exist during the different seasons of the population, which follows the intensive year (33). Thus, in the cool-temperate zones cropping of infested land with susceptible of the world (northern Europe or Ontario) cereal species, has been described from both where winter temperatures are low, It. field (39) and microplot experiments (37). avenae is able to over-winter as eggs within These results have also emphasized the cysts. By contrast, the infested areas of correlation between nematode population Australia experience a Mediterranean levels and yield loss. climate, and eggs remain quiescent through- Symptom expression in the seedling out a hot, dry summer and early autumn stage can be more accurately correlated with (fall). It is likely that eggs over-summer in larval populations than with cyst popula- other semi-arid climates, including India, tions. This relationship occurs because where spring cultivars are sown in autumn seedling growth may sometimes precede a and growth continues throughout a mild mass larval emergence so that plant growth winter. can be well established before a massive In Australia, crops are sown and larvae invasion of roots occurs (33, 35). In Aus- emerge after rains in late autumn, and soil tralia, disease may be minimized when temperatures are at the optimum range crops are sown soon after rain falls in (around 15 C) for hatching. In Europe, autumn. Crops sown some weeks later, in larvae emerge as temperatures rise in spring. late autumn or early winter, are often As a result, although the seasons in Aus- severely damaged. During the mild winter, tralia and northern Europe are opposite, which favors larval emergence, plant growth larval emergence takes place during the is slow and seedlings are less able to offset same months (33). In both of these situa- damage caused by the continual invasion tions, there is only one generation per year. of nematode larvae. In general, high temperatures (above Geographic and soil fertility differences: 20 C) do not favor the long-term survival The previously described relationships of H. avenae. In the laboratory, eggs in explain the reports that wheat is more cysts survive at high temperatures (21 C) severely damaged in Australia (34) and Cereal-Cyst Nematode: Meagher 13 India (42) than in Europe (17) or Canada to measure the potential for yield improve- (16). Winter are not grown in ment in wheat that might be achieved Australia but are commonly grown in either by the elimination of Europe and Canada where they escape through the use of nematicides (6) or the invasion during the winter months. In elimination of all soil-borne pathogens by Europe, however, spring wheat cultivars the use of a broad-spectrum fumigant may also be badly damaged (12). (chloropicrin 50 %, methyl bromide 50 %). Gair stated that, in this century, the The use of nematicides trebled grain yield nematode has caused increasingly more in comparison with yield on nontreated yield loss to crops in Europe because of the plots and CP, MeBr (450 kg/ha) produced more intensive cultivation of cereals (17). a four-fold increase (0.95 tonnes/ha to 4.02 Also, mechanization has increased the t/ha). Large yield increases have also spread and occurrence of the very suscepti- resulted from experiments with chemical- ble wild oat (54). Yield losses caused by H. control tests in India (42). The Australian avenae in Europe and Canada are much experiments were not planned to provide less than those in India or Australia where economic control, but the extent of the yield losses of 50% (51) or higher (6) are yield response obtained has stimulated often experienced, possibly because winter experimentation to test more economic wheat is usually grown in Europe and methods of chemical control. Canada and because barley cultivation has There is little doubt that the develop- increased. Barley cultivars are usually more ment of "resistant" wheat cultivars provides tolerant of invasion than spring wheat the greatest potential for economic control cultivars (34), except in India (31). In and yield improvement. In Europe, the addition, nematode resistance has been value of resistant barley cultivars is already bred into some European cultivars (8). accepted (9). In Australia, microplot experi- Other factors which may partially ac- ments have shown that yield increase is count for the observed differences in Europe possible by the use of trophic resistance. are: (i) higher soil fertility and the more This term is suggested to describe resistance widespread use of nitrogen fertilizer offsets to nematode reproduction rather than nematode symptoms; (ii) there is less mois- resistance to larval invasion and plant ture stress during the growing period and damage (trophos = feeding, reproduction). (iii) perhaps most important, wider crop Nevertheless, the danger exists that, rotatxons are more generally practiced. with incentives such as those provided by Nematode-fungus interaction: Research the "green revolution," it is possible that in Australia has shown that the most severe new cultivars may be introduced to a economic damage caused by H. avenae is region where the occurrence of H. avenae the result of nematode-fungus interactions is not recognized or that they may replace (35, 38). Because of its widespread occur- existing cultivars which possess tolerance. rence, solani Kiihn may be the For example, in India, some native cultivars most important fungus involved, but other are claimed to be tolerant (42), whereas cereal root-rot fungi may also be associated Australian experiments (5) indicate that in a root-rot complex (Meagher, unpub- some, and possibly all, of the high-yielding lished data). dwarf wheats are susceptible. This situation, combined with the more intensive cultiva- POTENTIAL FOR THE FUTURE tion of wheat, could lead to "genetic Heterodera avenae is now recognized as vulnerability," and it emphasizes the need one of the most important diseases limiting to evaluate all varieties to endemic path- wheat yields in southeastern Australia and, ogen populations (48). in future years, a similar situation may be Much is yet to be learned about the recognized in Rajasthan, India. Presently, occurrence of H. avenae biotypes in some we can only speculate on the likely spread regions (31), but it is hoped that cultivars of this species and the resultant yield effects produced from current breeding programs, that it will cause in the North American including those in Australia, might assist wheat belt. in providing healthy plants in a hungry In Victoria, Australia, we have attempted world. 14 Journal o/ Nematology, Volume 9, No. 1, January 1977

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