Population dynamics of the rice root nematode Hirschmanniella oryzae on monsoon rice in Myanmar

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1 Archives of Phytopathology and Plant Protection ISSN: (Print) (Online) Journal homepage: Population dynamics of the rice root nematode Hirschmanniella oryzae on monsoon rice in Myanmar Z.T.Z. Maung, P.P. Win, P.P. Kyi, Y.Y. Myint & D. De Waele To cite this article: Z.T.Z. Maung, P.P. Win, P.P. Kyi, Y.Y. Myint & D. De Waele (2013) Population dynamics of the rice root nematode Hirschmanniella oryzae on monsoon rice in Myanmar, Archives of Phytopathology and Plant Protection, 46:3, , DOI: / To link to this article: Published online: 20 Nov Submit your article to this journal Article views: 49 View related articles Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at Download by: [KU Leuven University Library] Date: 01 December 2015, At: 02:51

2 Archives of Phytopathology and Plant Protection, 2013 Vol. 46, No. 3, , Population dynamics of the rice root nematode Hirschmanniella oryzae on monsoon rice in Myanmar Z.T.Z. Maung a,c, P.P. Win a,c, P.P. Kyi a, Y.Y. Myint b and D. De Waele c,d,e * a Plant Protection Division, Myanma Agriculture Service, West Gyogone, Insein, Yangon, Myanmar; b Department of Plant Pathology, Yezin Agricultural University, Yezin, Myanmar; c Laboratory of Tropical Crop Improvement, Faculty of Bioscience Engineering, Department of Biosystems, University of Leuven (KU Leuven), Willem de Croylaan 42, 3001 Leuven, Belgium; d School of Environmental Sciences and Development, North-West University, Private Bag X6001, 2520 Potchefstroom, South Africa; e Crop and Environmental Sciences Division, International Rice Research Institute (IRRI), DAPO Box 7777, Metro Manila, Philippines (Received 11 October 2012; final version received 15 October 2012) Soil and root samples of the short crop cycle duration rice variety Yadanartoe were collected at 10-days intervals, starting at 20 days after transplanting until 20 days after harvest, from September 2008 until January 2009, to study the population dynamics of Hirschmanniella oryzae on (rainfed) monsoon rice. Plant growth stages, the ambient air and soil temperature, rainfall and relative humidity during the sampling period were noted. The soil type is clay and has a ph of 5.1. In the roots, three nematode population density peaks were observed during the sampling period: at the maximum tillering stage, at the milky grain stage, and between harvest and 10 days after harvest. The highest peak (483 H. oryzae/g roots) was observed at the milky grain stage. The lowest root population density (46 H. oryzae/g roots) was found at harvesting. Population densities in the soil followed more or less the same trend as in the roots. After harvesting, the soil population density increased. During our observation, we did not find any effects of environmental conditions on the population densities of H. oryzae. However, it was found that the population dynamics of H. oryzae were influenced by the plant growth stage. Keywords: environmental conditions; field study; plant-parasitic nematodes; Oryza sativa; population densities; rainfall, temperature Introduction Rice (Oryza sativa L.) is a tropical crop that can be grown under a variety of environmental conditions but is mostly grown in tropical regions with a hot and humid climate. The optimum temperature for rice cultivation is about 308C during the day and 208C during the night. Rice is being grown all over the world but Asia is the continent with the highest rice production. In 2008, Asia produced about 90% of the rice in the world (FAO 2009). In 2009, Myanmar produced almost 25 million tons of rice and it is one of the top 10 rice producing countries in the world (FAO 2009). The country benefits from a *Corresponding author. dirkdewaele@pandora.be Ó 2013 Taylor & Francis

3 Archives of Phytopathology and Plant Protection 349 tropical monsoon climate which is favourable for rice cultivation throughout the country. Throughout the country, annual rainfall and monthly average temperatures show considerable variation over time and place. In general, the climate is cooler in the highlands in the north and warmer in the Ayeyarwaddy River Delta in the south. The highest annual rainfall, ranging from 2500 to 5000 mm, occurs in the coastal and in the northern part of the country. In the central dry part of the country, the annual rainfall is lower than 1000 mm. The Ayeyarwaddy River Delta, comprising the Ayeyarwaddy, Yangon and Bago Divisions, has a fertile deltaic alluvial soil and abundant monsoon rainfall. It is the major rice producing area of the country. Plant protection is important worldwide for the production of rice because pathogens, including plant-parasitic nematodes, can be a major cause of reductions in rice yield and quality. Many nematode species have been reported being associated with rice but relatively few are considered of economic importance (Bridge et al. 2005). In Myanmar, an examination of 539 soil and 539 root samples of rice plants in 12 producing areas during the monsoon rice growing season in 2007 showed that the rice root nematode, Hirschmanniella oryzae, was the predominant nematode species attacking every monsoon rice variety examined (Maung et al. 2010). Previous studies, both under laboratory and field conditions, have indicated that soil moisture, soil type, soil ph, salinity, plant growth stage and crop cycle duration are the most important factors that affect the dynamics of H. oryzae populations on rice both in the soil and in the roots (Arayarungsarit and Junbuthong 1988; Hendro et al. 1992; Youssef 1998, 1999; Islam et al. 2004; Pokharel et al. 2004). A good knowledge of the population dynamics of a pathogen on a host plant in a specific environment may assist in making management decisions and in the more accurate timing of the application of a pathogen management practice (Trudgill and Phillips 1997). So far, no study has been undertaken to investigate the population dynamics of H. oryzae on monsoon rice in Myanmar. Therefore, a study was undertaken to examine the population dynamics of H. oryzae in a naturally infested field on Yadanartoe, a commonly cultivated monsoon rice variety. Materials and methods Description of the study site The study site, a farmer s field naturally infested with H. oryzae, was located in Padan village, Hlaingtharyar region in Yangon Division (Figure 1). This field was chosen as the study site because a high H. oryzae population density was detected when the survey was conducted during the 2007 monsoon rice growing season in addition to its long history of monsoon (rainfed) rice cultivation (Maung et al. 2010). Yangon Division is situated in the southern part of Lower Myanmar at about 15 m above sea level. This region has a tropical monsoon climate with a lengthy rainy season (from May through November) during which time a substantial amount of rainfall is received and a relatively short dry season (from December through April) during which time a limited amount of rainfall is received. During the rainy season, the average annual rainfall is 2620 mm. During the course of the year, average temperatures show little variation, with the average maximum temperature in the hottest months (March and April) ranging from 29 to 368C and the average minimum temperature in the so-called winter months (December to February) ranging from 18 to 258C. The soil type of this region is clay. Fallowing after monsoon rice

4 350 Z.T.Z. Maung et al. Figure 1. Site in Myanmar where the population dynamics study of Hirschmanniella oryzae on the rice variety Yadanartoe was carried out. production is the common cultivation method usually practiced by the farmers. In this region, rice has been grown for a decade or more. Manawthukha, Sinthwelatt and Taungpyan are the most popular and commonly grown rice varieties. In the previous years, the local variety Taungpyan was grown at the study site during the monsoon season. This rice variety has a long crop cycle duration (165 days). Starting from the 2008 monsoon season, the newly released short crop cycle duration rice variety Yadanartoe ( days) was planted. Transplanting was the common planting method used at the study site. Sampling and nematode population density assessment Soil and root samples of the rice variety Yadanartoe were collected from September 2008 until January Samples were taken at 10-days intervals, starting at 20 days after transplanting until 20 days after harvest. There were in total 14 sampling dates. Rhizosphere soil (150 ml soil at about 15 cm depth) and roots were collected from

5 Archives of Phytopathology and Plant Protection 351 one rice hill at 16 random sampling points in the field. Samples were stored in plastic bags in a coolbox until nematode extraction was carried out. The growth stage of the rice plants was recorded at each sampling date. Soil temperature at a depth of 10 cm was measured at five places in the field: four at the corners and one in the middle of the field. Soil texture, soil ph and organic matter content of the field were analysed in the laboratory of the Land Use Division, Myanma Agriculture Service, Yangon. The ambient air temperature, relative humidity and rainfall during the sampling period were obtained from the Mingaladon meteorology station, Yangon. While sampling, soil and root samples of barnyard grass (Echinochloa crusgalli) which was present in the field were also collected to examine for infection by H. oryzae. Samples were transported to the laboratory right after sampling and nematode extraction was processed on the same day of sampling. Nematodes from the soil samples were extracted by using Whitehead s tray method (Whitehead and Hemming 1965) and from the roots by a modified Baermann funnel method (Prot et al. 1993). The day after the extraction, the number of nematodes recovered from the samples was counted. The soil and root population densities of H. oryzae were expressed per 100 ml soil and 1 g fresh roots, respectively. Results The environmental conditions monitored during the duration of the sampling period at the study site are presented in Figure 2. The soil was acidic with a ph of 5.1 and had a clayey soil texture: 1.4% sand, 35.5% loam and 61.6% clay with 0.4% total N 2, 17.6 ppm P and 12.9 mg/100 g K 2 O. The relative humidity was high throughout the sampling period. The highest relative humidity (100%) was observed at the Figure 2. Average relative humidity, rainfall, soil and ambient air temperature observed during the different plant growth stages of the rice variety Yadanartoe in Padan village, Hlaingtharyar region, Yangon Division, Myanmar, from September 2008 to January 2009.

6 352 Z.T.Z. Maung et al. tillering stage and the lowest relative humidity (65%) at the dough grain stage. Because the sampling started during the late monsoon season, only 4 days with rainfall were noted: 3 days during the early growth stages, the 4th and last day during the heading stage. Soil temperature during the early growth to heading stage ranged from 24 to 288C. The lowest soil temperature (208C) was measured during the milky to harvesting stages. After harvesting at the last sampling time, the highest soil temperature (348C) was noted. The ambient air temperature did not fluctuate substantially during the whole duration of the sampling period (23 288C). The lowest air temperature (238C) was recorded at the first sampling and the highest air temperature (288C) was recorded at the late tillering stage. The average soil and root population densities of H. oryzae observed during the duration of the sampling period at the study site are presented in Figure 3. The population densities of H. oryzae observed in the roots showed three peaks during the duration of the observations. The first peak (200 H. oryzae/g roots) was observed at the maximum tillering stage of the rice plants. After this stage, the nematode population densities in the roots decreased until booting stage. Then, the nematode population densities increased sharply and the highest peak (483 H. oryzae/g roots) was found at the milky grain stage. Then, the nematode population densities in the roots decreased again and the lowest root population density (46 H. oryzae/g roots) was observed at the time of harvest. Between harvest and 10 days after harvest, the nematode population density in the roots increased again to peak at 318 H. oryzae/g roots. The population densities of H. oryzae in the soil followed more or less the same trend as the population densities in the roots. However, differences in the soil nematode population densities were low from the early growth stage until the booting stage. During plant growth, the highest population density in the soil (53 H. oryzae/100 ml soil) was observed at the heading and milky stages. After these stages, Figure 3. Population dynamics of Hirschmanniella oryzae observed on the different plant growth stages of the rice variety Yadanartoe in Padan village, Hlaingtharyar region, Yangon Division, Myanmar, from September 2008 to January 2009.

7 Archives of Phytopathology and Plant Protection 353 the population densities in the soil decreased first to increase again towards harvest when the highest soil population density (164 H. oryzae/100 ml soil) was observed. Hirschmanniella oryzae was also observed in the roots of barnyard grass at the study site. The average root population density of H. oryzae observed on this weed was 34 H. oryzae/g roots. Except H. oryzae, no other nematodes were observed in the samples of rhizosphere soil, rice roots and weeds. Discussion Throughout the duration of our study, the climatic conditions were ideal for rice growth and development. The ambient air temperature did not fluctuate substantially and was on average 258C. The soil temperature was high during the early growth stages (24 288C) and not lower than 208C at the milky to harvesting stages. The relative humidity was also high throughout the duration of the study. Rainfall was high during the early growth stages and although there were no rainy days during the later growth stages, enough water was retained in the field. Hirschmanniella oryzae completes part of its life cycle in the soil and, thus, its population dynamics is influenced by the soil environment including soil texture, soil ph, soil temperature and soil moisture, and root growth. The soil texture of our study site was clay and the average population density of H. oryzae in the soil observed was 53/100 ml soil. Hirschmanniella oryzae adapts better to clay soils than to sandy soils. In Senegal, the development of H. oryzae appeared to be better in clay soils (Fortuner 1977) and in India the highest H. oryzae population densities were observed in heavy clay soils (Mathur and Prasad 1971). The ph of our study site was 5.1. When the effect of ph on the activity and survival of three Hirschmanniella species was studied it was observed that H. oryzae survived very well at ph s ranging from 5 to 9 (Babatola 1981). Soil temperature is one of the most important environmental factors influencing the development of plant-parasitic nematode species. Youssef (1998) observed that there was a positive correlation between the root population densities of H. oryzae and soil temperature. Edward et al. (1985) mentioned that the optimal soil temperature for multiplication of H. oryzae was 21 to 288C. Throughout the duration of our study, the soil temperature at a depth of 10 cm in the field ranged from 20 to 348C while the average soil temperature was 24.68C. Throughout the duration of our study, the relative humidity was also high. At the late plant growth stages, the formation of new roots was observed. This new root formation may be a compensation for decayed roots. This observation supports the findings of Hollis (1967) who mentioned that H. oryzae caused decay of the tip of primary roots in soil with a high relative humidity. Yokoo and Su (1966) observed that populations of H. oryzae in the roots decreased rapidly after soil humidity has become lower. In our study, the population density of H. oryzae per g roots decreased from 230 to 46 when water from the field was drained for harvesting. However, high nematode population densities were again observed in the roots of the ratoons at 10 days after harvesting. At that time, more water was observed at the study site because water from the river near to the study site flooded the study site. This may have led to the formation of new roots and higher activity of the nematodes. Moreover, after harvest also high soil temperatures were observed at the study site. Pokharel et al. (2004) mentioned that the population dynamics of H. oryzae are also influenced by plant growth. In our study, the population densities of H. oryzae

8 354 Z.T.Z. Maung et al. were not very high in both soil and root samples at the early growth stages of the rice plants. Yokoo and Su (1966) observed that the population density of H. oryzae in the soil decreases after planting and increases after harvest when old roots start to rot. In our study, during the vegetative and reproductive period (from early growth to dough grain stage), a similar trend of H. oryzae population densities in the soil and the roots was observed. In our study, we found three peaks of H. oryzae populations in the roots samples. The first peak occurred at the tillering stage, the second and highest peak (483 H. oryzae/g roots) at the milky grain stage and the last peak at 10 days after harvesting. Our results confirm observations made by other rice nematologists. Wang et al. (1992) also reported three peaks of H. oryzae population densities on rice grown in the field. In Senegal, Fortuner (1976) observed that the highest percentage of the total H. oryzae population present in the roots of rice was found between the tillering and heading stages. Kuwahara and Iyatomi, cited by Fortuner and Merny (1979), reported that in Japan, the highest population density of H. oryzae in the roots of rice is observed at the heading stage irrespective of the date of planting. The same trend was also reported by Ramakrishnan (1992) who found that the population densities of H. oryzae were low after transplanting and reached a peak only at 60 days after transplanting. Previous studies mentioned that H. oryzae in rice roots leave the roots at the panicle initiation stage with a decline in the root population density at harvest (Hendro et al. 1992; Youssef and El-Hamawi 1996; Islam et al. 2004). This was the case in our study also: the H. oryzae root population density decreased sharply after the milky grain stage and the lowest population density was observed at the harvesting stage. From the dough grain to the harvesting stage, the population dynamics trend of H. oryzae in the soil was opposite with the trend in the roots. Starting from the maturity stage, the H. oryzae population in the soil increased and the highest soil population density was found at harvesting stage. Also, this observation agrees with previous observations. Only one peak of a H. oryzae soil population (at the harvesting stage) was observed when the short crop cycle duration rice variety RD25 was grown under field conditions in Thailand (Arayarungsarit and Junbuthong 1988). All observations suggest that during the later rice growth stages H. oryzae leave the decaying roots (Merny 1972; Arayarungsarit and Junbuthong 1988; Hendro et al. 1992; Youssef and El-Hamawi 1996; Youssef 1999; Islam et al. 2004). Taylor (1969) mentioned that H. oryzae does not migrate downward in the soil in between two successive growing seasons and that this nematode species is able to survive in situ during the dry season. When the rice plants reach maturity and the roots begin to lose vigour and decay, H. oryzae migrates en masse in the soil and may stay there for several months waiting for new host roots to feed (Walawala and Davide 1984). Results obtained by different authors indicate that several weeds of the Cyperaceae and Gramineae commonly found in rice fields are good hosts of H. oryzae. Barnyard grass is one of the weeds which can sustain high populations of H. oryzae (Mathur and Prasad 1973; Fortuner 1976; Babatola and Bridge 1979; Edward et al. 1985; Kumar 1990; Korayem 1993; Bridge et al. 2005). In our study, on average 34 H. oryzae/g roots were found in barnyard grass. As Anwar et al. (1992) pointed out, barnyard grass in rice fields may act as suitable alternative overwintering and summer hosts for H. oryzae.

9 Archives of Phytopathology and Plant Protection 355 Conclusion Throughout the duration of our study, the climatic and soil conditions were favourable for rice growth and for the development and reproduction of H. oryzae. Our observations confirm that the population dynamics of H. oryzae on rice are influenced by the plant growth stage. Both soil and root nematode population densities remained low during the early plant growth stages. The highest root population densities were observed at the milky growth stage. After the plant growth stage, H. oryzae migrated from the decaying roots in the soil. In addition to the favourable climatic and soil conditions, the long history of rice cultivation at the study site and the presence of barnyard grass in the rice field as a suitable alternative host for H. oryzae may result in a high initial nematode population density at the beginning of the next monsoon rice crop cycle. The present study was limited to only one field in only one region with only one rice variety due to the time limitation. To confirm the results of the present study, further studies need to be carried out in fields differing in environmental conditions, in different regions, with different rice varieties. Acknowledgements This research was made possible thanks to a Flemish Interuniversity Council (VLIR-UOS) PhD scholarship to Zin Thu Zar Maung. The authors also would like to thank the staff of the Myanma Agricultural Service in Yangon for their technical assistance and the local farmer of the study site for the permission to take samples. References Anwar SA, Rauf CA, Gorsi SD Weeds as alternate hosts of phytonematodes. Afro- Asian J Nematol. 2: Arayarungsarit L, Junbuthong S Population dynamics of rice root nematode Hirschmanniella oryzae in rice of different durations. Int Rice Res Newsl. 13:44. Babatola JO Effect of ph, oxygen and temperature on the activity and survival of Hirschmanniella spp. Nematologica. 27: Babatola JO, Bridge J Pathogenicity of Hirschmanniella oryzae, H. spinicaudata, and H. imamuri on rice. J Nematol. 11: Bridge J, Plowright RA, Peng D Nematode parasites of rice. In: Luc M, Sikora RA, Bridge J, editors. Plant parasitic nematodes in subtropical and tropical agriculture, 2nd ed. Wallingford (UK): CAB International. p Edward JC, Sharma NN, Agnihothrudu V Rice root nematode (Hirschmanniella spp.) A review of the work done in India. Curr Sci. 54: FAO FAOSTAT database [Internet]; [cited 2012 Oct 2012]. Available from: faostat.fao.org/site/567/default.aspx#ancor. Fortuner R Les ne matodes parasites des raciness associee s au riz au Se ne gal. Thèse Docteur-Inge nieur, Universite Cl. Bernard, Lyon, France, No. 249, 51 p. Fortuner R Fertilization du riz et de gats cause s par le ne matode Hirschmanniella oryzae (van Breda de Haan) Luc & Goodey. Proce` s-verbal de la séance du 1ier Juin, 1977, Acade mie d Agriculture de France 58: Fortuner R, Merny G Root-parasitic nematodes of rice. Rev Ne matol. 2: Hendro SME, Prot JC, Madamba CP Population dynamics of Hirschmanniella mucronata and H. oryzae on Sesbania rostrata, Aeschynomene afraspera and rice cv. IR 58. Fund Appl Nematol. 15: Hollis JP Nature of nematode problem in Louisiana rice fields. Plant Dis Rep. 51: Islam MS, Ahmad MU, Haque AH.M, Sarker MEH Population dynamics of Hirschmanniella oryzae in the rice roots of farmer fields as affected by edaphic factors. Pakistan J Biol Sci. 7:

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