The Relationship Between Enosima Leucotaeniella and Barnyard Grass, and the Potential of E

THE RELATIONSHIP BETWEEN ENOSIMA LEUCOTAENIELLA AND BARNYARD GRASS, AND THE POTENTIAL OF E. LEUCOTAENIELLA AS A BIOLOGICAL CONTROL

Michiyo Goto Faculty of Agriculture, Yamagata University Tsuruoka, Yamagata 997, Japan

ABSTRACT

E. leucotaeniella is a moth, the larva of which is a selective stemborer. It has a characteristic life cycle closely related to that of Echinochloa. E. oryzicola and E. crus-galli var. crus-galli were observed in paddy fields of Japan. Plants of both species were infested with E. leucotaeniella. Damage was observed in E. oryzicola only at its vegetative stage, and was not observed at all in E. crus-galli var. crus-galli. The specificity of E. leucotaeniella damage to E. oryzicola and E. crus-galli var. crus-galli was investigated in relation to the ecological and physiological characteristics of the two weed species.

INTRODUCTION many problems have to be solved. In the present paper, the relationship between Echinochloa and E. It has been suggested that Echinochloa leucotaeniella is described. In addition, the poten- weeds are no longer a problem in Japan. However, tial of E. leucotaeniella as a biological control agent if herbicides cease to be applied to paddy fields these is discussed. soon become covered with Echinochloa (Iwasaki, 1985). Hence, Echinochloa weeds may only be RELATIONSHIP BETWEEN E. temporarily suppressed by herbicides. Not only LEUCOTAENIELLA AND ECHINOCHLOA herbicides but also various integrated control meth- ods such as biological control should be used to A survey was carried out of three crops, regulate these weeds. rice (Oryza sativa), Japanese barnyard millet The starting point for the biological control (Echinochloa utilis) and corn (Zea mays), with of a weed in paddy fields is to find a selective regard to infestation by 43 weed species belonging to biological agent against it which leaves the rice crop 16 families. Infestation with stemborer was found intact. So far, with regard to biological agents for only in Echinochloa, namely E. utilis, E. oryzicola Echinochloa weeds, it is known that grass carp and E. crus-galli var. crus-galli (Goto 1977). The (Ctenophryngodon idella) and red tilapia relationship between E. leucotaeniella and (Tilapiamossambica XT. nilotica-anrea) (Itoh et al. Echinochloa is presented in Fig. 2. Echinochloa 1991b) and a planthopper, Sagatodes pusanus species are characterized by four main features (Mohamed et al. 1986), all have the potential to namely; control weeds. However, they are not selective. E. • Numerous narrow stems, leucotaeniella is a moth (Fig. 1), the larva of which • The stem is enclosed by a hard outer is a selective stemborer which infests only layer, Echinochloa (Goto 1977). It was discovered in • Leaf development is divided into two 1974 in the stem of barnyard grass growing in a rice phases, and nursery in Shonai District, Yamagata Prefecture, in • They have a submerged habitat. northern Japan. Before E. leucotaeniella can be These characters are closely related to the life used as a biological control agent of Echinochloa, cycle of E. leucotaeniella.

Key words: barnyard grass: Echinochloa: E. crus-galli var. crus-galli: E. oryzicola: E. leucotaeniella: paddy weeds 1 Fig. 1. Male (left) and female (right) of E. leucotaeniella

Numerous Narrow Stems immediately after hatching and developed into pupae, with a high survival rate. Hence, the inside of The spatial distribution of E. leucotaeniella the stem may be a safe haven for E. leucotaeniella. larvae per plant and per stem were investigated in E. On the other hand, the behavior of hatch- oryzicola growing in open paddy fields. The data ing, eclosion, oviposition and copulation occurs were analyzed using the m-m method (Iwao 1968). outside the stem, and circadian rhythms can be The results showed that most infestation consisted of observed in these behavior (Fig. 1; see also Goto one larva per stem, equivalent to a uniform distribu- 1979, Goto et al. 1989). Each peak of the circadian tion pattern (Goto 1985c). Dispersed hatching rhythms occurred at different times and under differ- behavior may be a cause of this uniform distribution, ent conditions, according to the growing stage of the which may be an advantage in that each larva can larvae. E. leucotaeniella may in this way be able to develop without competition. On the other hand, the avoid various unfavorable environmental conditions distribution pattern of larvae in individual plants was occurring outside the stem. recognized as aggregative, which indicated that the larvae might have begun as a clump. This aggregative Two-Phase Leaf Development nature may come from egg mass deposition on the plant, as is the characteristic mode of moth repro- The leaf development of Echinochloa can duction. The egg mass size of E. leucotaeniella was be divided into two phases, vegetative and reproduc- small, with an average of only 13 eggs (Goto 1978). tive. The stem during the vegetative phase is short The size of the egg mass is closely related to the and weak, but during the reproductive phase it number of Echinochloa stems. Hence, the survival becomes long and robust. The diapause rate of E. rate of eggs might be regulated by the number of leucotaeniella increases as Echinochloa passes into stems, in that each hatching larva needs one stem in the reproduction phase (Fig. 3). In plants at the same order to survive. leaf stage, the diapause rate was higher among larvae in E. crus-galli var. crus-galli than among those in Habituation in the Stem E. oryzicola. During the vegetative phase, the entire stem of Echinochloa is eaten by the larvae, so that E. leucotaeniella larvae entered the stem the stem soon dies. During the reproductive stage,

2 Fig. 2 The relationship between E. leucotaeniella and Echinochloa

the stem survives because it is only partially eaten. the larva eats the leaf tissue it moves down to the base of the leaf, which it soon enters. In moving through Submerged Habitat of Echinochloa the stem, the larva does not make any hole to the outside, so water around the plant does not infiltrate Echinochloa is a well-known weed in rice through the stem. Before pupation, E. leucotaeniella fields (Yubuno 1975) or in swamps and other aquatic larvae make a hole in the stem from which the moths habitats (Holm et al. 1977). E. leucotaeniella exhib- later emerge. However, the hole is still covered by its moisture tolerance throughout its various stages the epidermal layer of the stem, so that water does of development (Table 1). The egg mass is ovipos- not infiltrate through the hole. When stems infested ited at the leaf tip, and hatching normally occurs even with pupae were put under water, eclosion occurred if the leaf is submerged. After hatching, the larvae normally and the moths flew out from the stem immediately disperse and enter the leaf sheath. As through the water into the air. Thus, E. leucotaeniella

3 Fig. 3. Relationship between the leaf stage and rate of diapause

Source: (Goto 1985)

can be seen to exhibit high moisture tolerance from Echinochloa species, newly hatched larvae of E. the egg to the moth stage. E. leucotaeniella may in leucotaeniella were inoculated in Echinochloa spe- fact be the only stemborer which can use submerged cies. The results are presented in Fig. 4. There was Echinochloa stems. no significant difference in the dry weight of shoots and seeds between inoculated and control (non- RELATIONSHIP BETWEEN E. inoculated) at any stage of E. crus-galli var. crus- LEUCOTAENIELLA AND galli. However a significant difference was found ECHINOCHLOA SPECIES between inoculated and non-inoculated plants of E. oryzicola at the 6th and 10th leaf stages. The rate at The ecological and physiological proper- which stems were eaten by the larvae, and the ties of the two species E. crus-galli var. crus-galli occurrence of leaves with signs of feeding, are and E. oryzicola are presented in Table 1 (Goto presented in Fig. 5. The feeding pattern is marked 1985b). Weeds can be defined as organisms adapted only as present or absent. When the two Echinochloa to habitats frequently disturbed by man (Oka 1983). species were compared, 100% of plants at the Ehrendorpher (1965) has pointed out several fea- vegetative stage showed signs of having been eaten. tures common to weeds, such as the prolonged Damage to E. oryzicola was very marked because period before seed emergence, rapid plant develop- the entire stem had been eaten. Stem elongation ment, a wide range of phenotypic plasticity and wide began after phase conversion, which occurred at seed dispersal. E. crus-galli var. crus-galli pos- about the 11th stage in E. oryzicola and the ninth sesses at least two features characteristic of weeds, stage in E. crus-galli var. crus-galli. E. oryzicola i.e. fast development at the early stage of plant has a prolonged vegetative period, so that it is growth, and conversion from the vegetative to the exposed to infestation over a long period. E. crus- reproductive phase at an early stage, resulting in galli var. crus-galli, on the other hand, developed early maturity. The plants are tall and robust, rapidly at the early growth stages, so it was able to producing large numbers of small, long-awned seeds. recover from any serious damage received during its E. oryzicola, on the other hand, has several charac- vegetative phase. teristic features which mimic rice (Morinaga et al. The relationship between E. leucotaeniella 1942), i.e., prolonged seed germination, slow devel- and Echinochloa weeds is summarized in Table 2. E. opment at the early growth stages, belated phase oryzicola was attacked by E. leucotaeniella at the conversion, and a weak, narrow stem. vegetative stages. Since the vegetative stage of this In order to assess the potential of E. weed species is longer than that of E. crus-galli var. leucotaeniella in the biological control of crus-galli, there was severe damage due to the long 4 Table 1. Comparison between the ecological and physiological properties of E. oryzicola and those of E. crusgalli var. crusgalli

Source: Goto 1985b

5 Fig. 4. Relationship between leaf stage and dry weight in pot

Fig. 5. Rate at which the stem is eaten by E. leucotaeniella, and rate of occurrence of leaves used as food

6 period of infestation. Since E. crus-galli var. crus- Fiji. As a result, a tremendous increase in the galli entered the reproductive stages earlier than E. population of grassy weeds, especially Echinochloa, oryzicola, E. leucotaeniella consequently entered has been noted (Itoh 1991a). Paddy fields with a diapause at an early stage. In Shonai District, moths serious infestation of barnyard grass in Peninsular belonging to the 3rd generation sometimes emerged Malaysia had a yield reduction of as much as 41% (Goto 1985a). These were probably emerging from (Azmi 1985). There are five species of Echinochloa E. oryzicola. During the reproductive stage of both in the rice fields of Malaysia, namely the E. crus-galli Echinochloa species, 4th instar larvae were found to complex, E. oryzicola, E. stagnina, E. picta and E. have a high rate of movement in E. oryzicola, and the colona (Itoh 1991b). E. stagnina and E. picta are mortality of late instar larvae was high. The site for perennial, while the three other species are annual making a cocoon for diapause larvae was regularly weeds. A survey of five Echinochloa species in found at the stem node of E. oryzicola, but there was Malaysia found that four of them were infested with no regular site for cocoons in E. crus-galli var. crus- E. leucotaeniella. Infestation with E. picta was galli. Although E. leucotaeniella is well adapted to particularly heavy. However, no infestation was Echinochloa, it causes so much damage to the weed found of E. colona or of rice. as to decrease its own survival rate. Probably the It is important that the stemborer entered special vulnerability of E. oryzicola is due to changes into stems, not only of annual but also of perennial from weedy features to characters mimicking rice. species, because new stems from perennial species This artificial selection took place during the rela- are present throughout the year to serve as food for tively short period that rice has been cultivated, the stem borer. This means that a high moth density while Echinochloa and E. leucotaeniella have prob- can be maintained throughout the year. ably coexisted for a very long time. The changes in Intensive programs to use Echinochloa as the characteristic features of E. oryzicola have made a biological control agent can be expected in the it a weed which is difficult to control, but these may future. These will both ensure that there is a food assist the stemborer to control it more easily. In supply for the stemborer throughout the year, and recent years, direct seeding of rice has been replacing synchronize the period of oviposition of E. direct transplanting of rice in the irrigated fields of leucotaeniella with the vegetative stage of Thailand, the Philippines, Sri Lanka, Malaysia and Echinochloa plants.

Table 2. Relationship between E. leucotaeniella and two Echinochloa species

7 REFERENCES Goto, M. 1989. Ecological study on a barnyard grass stem borer, Emmalocera Azmi, M. 1985. Weed Problems and their sp.. VI. Control of hatching time of Management in Direct Seeded Rice. Rice eggs. Japanese Journal of Applied Ento- Division, MARDI Seberang Perai. 19 pp. mology and Zoology 33: 115-121. (In (In Bahasia Malaysia). Japanese). Ehrendorfer, F. 1965. Dispersal mechanisms, Holm, L.G., D.L. Plucknett, J.V. Pancho and genetic systems, and colonizing abilities in J.P. Herberger. 1977. The World’s some flowering plant families. In: The Worst Weeds: Distribution and Biology. Genetics of Colonizing Species, H.G. East-West Center, University of Hawaii Baker and G.L. Stebbins (eds.). Aca- Press, Honolulu. 609 pp. demic Press, New York, pp. 331-352. Itoh, K. 1991a. Integrated weed manage- Goto, M. 1977. Ecological studies on ment of direct seeded wet rice fields in Emmalocera sp. parasitic to Echinochloa. South East Asia and Pacific Regions, with I. Development of immature stages and special reference to Malaysia. 13th Asian seasonal emergence of adults at Yamagata Pacific Weed Science Society Proceedings Prefecture. Journal of Yamagata Agricul- 1: 77-94. ture and Forestry Society 34: 29-34. Itoh, K. 1991b. Life Cycles of Rice Field (In Japanese). Weeds and their Management in Malay- Goto, M. 1978. Ecological studies on sia. Tropical Agriculture Research Cen- Emmalocera sp. Parasitic to Echinochloa. ter. 89 pp. II. The variation of egg mass size and Iwao, S. 1968. A new regression method oviposition site of the egg. Journal of for analyzing the aggregation pattern in Yamagata Agriculture and Forestry Soci- animal populations. Research Population ety 35: 1-3. (In Japanese). Ecology 10: 1-20. Goto, M. and T. Yamada. 1979. Ecological Iwasaki, K. 1985. Physiological and ecologi- studies on Emmalocera sp. parasitic to cal studies on the control of paddy field Echinochloa. Daily behavioral rhythms in Scirpus weeds, so-called “Hotarui”. Weed adult stage and experimental studies of Research 30: 93-106. (In Japanese). the timing mechanism of oviposition. An- Mohamed, M.S. and B. Abd. Hamed. nual Report, Plant Protection of North 1986. Occurrence of Sogatodes pusanus Japan 30: 6-11. (In Japanese). (DISTANT) (Homoptera: Delphacidae) in Goto, M. 1985a. Ecological study on a the rice ecosystem of Tanjong Karang. barnyard grass stem borer, Emmalocera MARDI Research Bulletin 14: 271-274. sp.. IV. Effects of day-length and host Morinaga, T. and T. Nagamatsu. 1942. plant on the onset of larval diapause. Genecological studies on barnyard grass Japanese Journal of Applied Entomology in paddy fields. Ikusyu Kenkyu 1: 116- and Zoology 29: 298-303. (In Japa- 122. (In Japanese). nese). Oka, H.I. 1983. Life-history characteristics Goto, M. 1985b. Physiological and ecologi- and colonizing success of plants. Ameri- cal properties of Echinochloa species in a can Zoologist. 23: 99-109. paddy field of the Shonai District. Weed Yoshiyasu, Y. 1993. Redescriptions of the Research 30: 270-276. (In Japanese). genus Enosima Stat. nov. and E. Goto, M. 1985c. Ecological study on a leucotaeniella comb. nov., with notes on barnyard grass stem borer, Emmalocera the immature stages (Lepidoptera, sp., in a paddy field. V. Pattern of spa- Pyralidae). Japan Jour. Entomology 61. tial distribution for immature stages of a (In press). barnyard grass stem borer Emmalocera Yubuno, T. 1975. The classification and sp., in a paddy field. Journal of geographical distribution of the genus Yamagata Agriculture and Forestry Soci- Echinochloa. Weed Research 20: 97- ety 42: 27-33. (In Japanese). 104. (In Japanese).

8 DISCUSSION

Dr. Banpot commented that a different species of the same genus Emmalocera* is a stem borer pest of sugarcane in India. He recommended that great care should be taken in introducing it as a weed control agent, to prevent any unwanted effects on non-target species. Dr. Goto was asked whether other species of insect are known to attack barnyard grass in Japan. He replied that there are a number of natural enemies, including the Oriental corn borer, but this also attacks crops.

Dr. Mochida enquired whether Dr. Goto had attempted the mass production of E. leucotaeniella. Dr. Goto replied that some work had been done on this, but that there were still considerable difficulties.

Dr. Kim was interested in the possibility of differences in the response to E. leucotaeniella in different rice varieties. Even if E. leucotaeniella were to give good control of barnyardgrass, he felt there might be a danger that some rice varieties would be susceptible. Dr. Goto agreed that thorough testing would be necessary, and felt that this should cover the feeding behavior of the larvae as well as the ovipositing behavior of the female, to see whether the species is sufficiently closely adapted to Echinochloa. He added that numerous host feeding tests using many different plant species had failed to show that E. leucotaeniella had any other host plant than Echinochloa.