Leersia hexandra, a weed host of the rice brown planthopper, Nilaparvata lugens (Stål)

CROP PROTECTION (1984) 3 (1), 77-85

Leersia hexandra, a weed host o f the rice brown planthopper, Nilaparvata lugens

(StM) E. A. HEINRICHS AND F. G. MEDRANO

Department of Entomology, International Rice Research Institute, PO Box 933, Manila, Philippines ABSTRACT. A population of the rice brown planthopper, Nilaparvata lugens (Still) (Homoptera: Delphacidae), was abundant on a weed, Leersia hexandra, growing in irrigation canals near rice fields in the Philippines. When individuals of this population were placed on rice, Oryza sativa, feeding was low and they could not survive. Conversely, L. hexandra was not a host for the N. lugens population maintained on rice. Although the two N. lugens populations differed in feeding behaviour, under 'no choice' conditions in the greenhouse they interbred and produced progeny which could utilize both L. hexandra and O. sativa as a host. The Leersia population is important in the management of N. lugens on rice as it is attacked by the same predators, parasites and pathogens as the rice population.

Introduction

Leersia hexandra is a weed that is commonly found in irrigation canals which supply water to lowland rice fields in Asia. A population morphologically the same as the rice brown planthopper, Nilaparvata lugens (St~l) (Homoptera: Delphacidae), was discovered on L. hexandra at the International Rice Research Institute (IRRI), Luzon, Philippines. This was of special interest because N. lugens is generally considered to be restricted to cultivated rice, Oryza sativa, and wild rices, Oryza species. T h e host range o f N . lugens as discussed in the literature is inconclusive because of discrepancies in the definition of what constitutes a host. In a review of the literature Chen (1982) found that at least 103 plant species within seven families had been reported as 'hosts'. Among these are cultivated rices, wild rice species, grasses, broad-leaved weeds, wheat, sugar-cane and others. Most of the literature deals with field collections of N. lugens without proof that it can survive and multiply on the source from which it was collected. Some authors refer to hosts as plants on which N. lugens oviposits and survives for a portion of the life cycle. However, the only host other than Oryza spp. on which N. lugens has been shown to be able to complete its 0261-2194/84/01/0077-09503.00© 1984Butterworth& Co (Publishers)Ltd

78

N. lugens hosts

life cycle is L. hexandra; however, reports (Lei, Liu and Wu, 1982; Shou and Gong, 1982) indicate that it is not a highly suitable host compared with rice. In China, where there is interest in determining whether N. lugens can overwinter on weeds when rice is not available, Lei and Wang (1958) found that N. lugens passes the winter in the egg stage in L. hexandra and other weeds along the edges of streams. Lei et al. (1982) reported that a few N. lugens could complete their life cycle on L. hexandra. However, survival increased when rice was occasionally supplied as a food source. In addition, the nymphal development period of survivors was longer and adult life span shorter when feeding on only L. hexandra compared with feeding alternately on rice and L. hexandra. Similar results were obtained by Shou and Gong (1982) where only 2~o of the nymphs survived to the adult stage. In laboratory tests at IRRI (1979) and in Indonesia (Oka, 1979) no nymphs survived to become adults on L. hexandra. Investigations were conducted to determine if L. hexandra could serve as an alternate host for populations ofN. lugens. Availability ofL. hexandra as an alternate host is important for several reasons. The weed may serve as a reservoir for potential infestation during the season when rice is not cultivated and as a reservoir of N. lugens predators, parasites and pathogens. In addition, the L. hexandra populations could affect the rate of biotype selection by contributing genes for avirulence to the gene pool. For these reasons, greenhouse studies were conducted to determine the suitability of L. hexandra and rice as hosts for the L. hexandra (Leersia) population and L. hexandra as a host for the rice N. lugens populations maintained in the greenhouse. Materials and methods The Leersia population was identified as N. lugens by IRRI taxonomists, and also confirmed as morphologically N. lugens by M. F. Claridge of University College, Cardiff, UK. Test insects of the Leersia population were obtained by collecting from L. hexandra in irrigation canals adjacent to rice fields on the IRRI farm. These populations were then reared on potted L. hexandra cuttings in the greenhouse for one generation. The rice population was obtained from cultures originally collected from rice in the field and maintained on rice in the greenhouse for more than 50 generations. All tests were conducted in the greenhouse at a temperature of 20-35°C.

Longevity and fecundity of Leersia and rice adults The first test was conducted to determine whether there was any difference in the longevity and fecundity of the Leersia populations and biotype 1 rice population on their respective hosts, L. hexandra and TN1 rice variety. One pair (male and female) of 1-day-old adults were placed on potted plants covered with a cylindrical Mylar film cage. Each of the two treatments was replicated 10 times, one potted plant serving as a replicate. At 5-day intervals the adults were transferred to fresh potted plants. Newly hatched nymphs were counted daily and removed from the cage. Twelve days after the female in each cage died, the plants were dissected and unhatched eggs counted. Fecundity was based on the sum of the nymphs and unhatched eggs. Date of death of each adult male and female was recorded to determine longevity.

E. A. HEINRICHSAND F. G. MEDRANO

79

Feeding activity, incubation period and hatchability This test was designed to determine the suitability of the two hosts, L. hexandra and TN1 rice variety for the Leersia and biotype 1 N. lugens populations. Feeding activity was determined by placing five 3- to 4-day-old adults in a feeding chamber as described in Paguia, Pathak and Heinrichs (1980). Filter papers used to collect the honeydew were treated with a bromocresol green solution prior to placement in the chamber. The area of the spot produced by reaction of the honeydew with the bromocresol green was measured to determine feeding activity (Pathak and Heinrichs, 1982b). Treatments were replicated six times. Eggs laid by the adults during the feeding study were used to determine the incubation period and percentage hatchability. When the feeding study was completed the feeding chamber was removed and the plants enclosed with cylindrical Mylar film cages. Hatching nymphs were recorded and removed daily. Eleven days after the adults were removed the plants were dissected and the unhatched eggs counted. Percentage hatchability was determined by: Number of nymphs x 100 Number of n y m p h s + n u m b e r of unhatched eggs

Survival of rice biotypes on L. hexandra Three distinct N. lugens populations or biotypes with respect to virulence are maintained at IRRI. Biotype 1 is the general population which can only feed on varieties with no genes for N. lugens resistance whereas biotype 2 is virulent to varieties possessing the Bph 1 and biotype 3 to varieties possessing the bph 2 gene for resistance (Pathak and Heinrichs, 1982a). Biotypes 1, 2, and 3 were reared on varieties TN1 (no gene), Mudgo (Bph 1 gene) and ASD7 (bph 2 gene), respectively. The Leersia population served as a check. Treatments were replicated 10 times, each potted plant consisting of one replicate. Potted plants were caged with Mylar film and 100 newly hatched nymphs placed in each cage. At 15 days after infestation the number of living insects in each cage was recorded.

Survival of the Leersia N. lugens population on resistant and susceptible varieties Seven rice varieties with various genes for rice N. lugens resistance were tested to determine their suitability as hosts for the Leersia population. Varieties tested and their respective resistance genes are given in Table 2. L. hexandra was included as a check (control). Ten newly hatched Leersia nymphs were caged on 35-day-old potted test plants. The number of live insects was recorded 10 days after infestation.

Feeding activity of the Leersia population on resistant and susceptible rice varieties Test varieties were the same as described for the previous test. L. hexandra served as the check. The procedure followed to determine feeding activity was the same as in the previously described feeding activity study.

Interbreeding of the Leersia and rice populations The Leersia and rice populations were separately reared on their respective host

80

N. lugens hosts

plants L. hexandra and TN1 rice growing in test tubes. Adults emerging on the same day were used in making crosses between the two populations. Crosses were made by placing one male and one female in a cage Containing both L. hexandra and TN1 plants. Crosses consisted of the Leersia female and rice biotype 1 male, and its reciprocal. Each cross was replicated 10 times. The newly hatched nymphs (FI progeny) from each cross were placed on L. hexandra or T N 1 plants and survival recorded at 13 days after infestation. Survival of the progeny wa s compared with that of the checks consisting of the parents, Leersia and rice biotype 1 populations on L. hexandra and TN1. Leersia population as a host for natural enemies Five tests were conducted to determine the suitability of the Leersia population as a host for the major predators, parasites and pathogens attacking the rice biotype 2 N. lugens population.

Predators. Percentage predation by the spider, Lycosa pseudoannulata ofN. lugens adults and by the mirid bug, Cyrtorhinus lividipennis on N. lugens eggs was studied in separate tests. In the L. pseudoannulata test, 10 Leersia N. lugens female adults were introduced into cages containing 40-day-old L. hexandra plants, and 10 rice N. lugens female adults were placed in cages containing 40-day-old TN1 rice plants. The next day dead N. lugens were replaced and then one L. pseudoannulata adult was released into each cage. Caged plants ofL. hexandra and TN1 with Leersia or rice N. lugens without spiders served as checks. Five days after placing L. pseudoannulata in the cages the number of living N. lugens in each cage were counted. Each treatment was replicated 10 times. In the C. lividipennis test five gravid rice N. lugens females were placed on caged TN1 plants and five gravid Leersia N. lugens placed in a cage containing L. hexandra plants. After a 24 h oviposition period the N. lugens were removed and five fourth-instar C. lividipennis nymphs placed in each cage. Five days later plants were dissected and the number of eggs fed on by C. lividipennis and undamaged eggs was recorded. Each treatment was replicated 12 times.

Parasites. Two parasites, an egg parasite, Anagrus sp., and a nymphal parasite, a dryinid, Pseudogonatopus nudus, were tested on the two N. lugens populations. In the Anagrus test five gravid Leersia N. lugens females were introduced into a cage of potted L. hexandra plants and five gravid rice N. lugens were placed in a cage of TN1 plants. After a 24 h oviposition period the N. lugens were removed and 100 Anagrus adults reared on rice N. lugens eggs were placed in each cage. The Anagrus adults were removed after five days. Hatching nymphs representing unparasitized eggs were counted 10 days after Anagrus adults were removed. Emerging parasites were counted 15 days after infestation with the Anagrus adults. Plants were then dissected and the parasitized eggs from which adult parasites failed to emerge and unparasitized-unhatched eggs were counted. Each of the caged plants represented a replication and each treatment was replicated 10 times. In the dryinid study, 20 third-instar Leersia N. lugens nymphs were placed in a cage containing potted L. hexandra plants and 20 rice N. lugens nymphs were placed in a cage with potted TN1 plants. Each potted plant consisted of a replication and each treatment was replicated 12 times.

E. A. HEINRICHSAND F. G. MEDRANO

81

One day after N. lugens infestation, one gravid dryinid female was placed in the cage and removed 24 h later. T h o s e N. lugens fed upon and killed by the dryinid were counted and removed daily for five days. On the 6th to 10th day after the infestation with a dryinid, N. lugens with a P. nudus larva seen protruding from the abdomen were counted.

Pathogens. Susceptibility of the two N. lugens populations to Metarrhizium anisopliae and Beauveria bassiana was determined in one test. Potted L. hexandra and T N I plants were sprayed with a 2 ml water suspension of the fungal spores. Immediately after spraying, the plants were enclosed in Mylar film cages and 20 third-instar Leersia and rice N. lugens nymphs were placed on their respective host plants. Beginning 24 h after infestation, dead N. lugens were collected daily with the aid of a sterilized forceps and placed on moist filter paper in a Petri dish. After a 24 h sporulation period the insects were examined under a microscope to verify whether they were infested with the fungus. T r e a t m e n t s were replicated five times.

Results T h e longevity of the Leersia females and males on L. hexandra was similar to that of the rice population on T N 1 (Table 1). Fecundity of both populations on their respective host plants was high with the rice population producing significantly more eggs. Both populations actively fed on their respective host plants but feeding activity of the rice biotype 1 population on T N 1 was twice that of the Leersia population on L. hexandra (Table 1). However, feeding activity of the Leersia population on T N 1 and rice population on L. hexandra was the same. Egg hatchability of the Leersia population on L. hexandra and T N 1 were similar. However, hatching of the rice population on L. hexandra was decreased, being only 48~o, whereas it was 92% on TN1. Leersia hexandra was completely unsuitable as a host for the nymphs of the three TABLE 1. Biological aspects and feeding activity of the Nilaparvata lugens, Leersia and rice biotype 1 populations on L. hexandra and rice (TN1) plants.t IRRI greenhouse, 1982. Leersia p o p u l a t i o n on:

Rice p o p u l a t i o n on:

Parameters

L. hexandra

TN1

L. hexandra

TN1

Adult longevity (days) Female Male Fecundity (eggs/female) Feeding (honeydew spot in m m 2) Incubation period (days) Egg hatch (%)

32"8 a 27.2 a 513-0 b 493-6 b 7"8 a 81.2 a

---50"9 c 7.8 a 77.5 a

---119"1 c 7-8 a 47"8 b

34"4 a 31.7 a 672-0 a 1162-6a 7"5 a 92.4 a

t Means within a row followed by a common letter are not significantly different at the 5% level by Duncan's multiple range test.

N. lugens hosts

82

rice biotypes as there was no survival. In the same test, survival of the Leersia population on L. hexandra was 750/0 . N o n e of the rice varieties with the various genes for N. lugens resistance were suitable hosts for the Leersia population. T h e r e was no survival of nymphs on T N 1 , with no gene for resistance, or on any of the varieties with different resistance genes (Table 2). Survival on L. hexandra, however, was 88~/o. Feeding of the Leersia population on the same varieties was low (Table 2). T h e area of the spots produced by the honeydew excreted by the Leersia population on the rice varieties was one-sixth that on L. hexandra. In addition, all of the spots produced from honeydew of the hoppers feeding on the rice varieties were white, whereas 80~o of the spot area on the L. hexandra treatment was a dark blue colour. In feeding studies on the green leaf hopper, Nephotettix virescens, on rice white spots were produced when feeding on resistant varieties on which the leaf hoppers could not survive (Auclair, Baldos and Heinrichs, 1982). H o n e y d e w analysis indicated xylem feeding on the resistant varieties, whereas phloem feeding (resulting in dark blue spots on bromocresolgreen treated filter paper) was most common on susceptible varieties. It thus appears that the Leersia population cannot feed in the nutrient-laden phloem of the rice varieties but does feed on the phloem of L. hexandra. T h e Leersia and rice populations freely interbred and produced viable progeny when caged together in the absence of mate choice in the greenhouse. Survival of the F1 progeny on L. hexandra and T N 1 differed from that of the parents (Figure 1). Survival of the progeny of both crosses was intermediate between that of the parents on the two hosts. Survival was slightly higher on T N 1 than on L. hexandra. Both populations were attacked by the predators, parasites and pathogens (Figure 2). L. pseudoannulata predation was highest on the Leersia N. lugens, whereas C. TABLE 2. Survival of Leersia Nilaparvata lugens nymphs and amount (mm 2) of honeydew excreted by Leersia female adultst when feeding on rice varieties with rice N. lugens resistance genes and on Leersia hexandra. IRRI greenhouse, 1982.

Treatment

Resistance gene(s)

Survival (%)

Area of honeydew spots on filter paper (mm2)~

63 a 65 a

Rice TN1 Mudgo

None Bph 1

0a 0a

IR26

Bph 1

0a

58 a

ASD 7 Rathu Heenati Babawee Ptb 33

bph 2 Bph 3 bph 4

0a 0a 0a 0a 88 b

53 a 57 a 46 a 54 a 315 b

Leersia hexandra (check)

2 unnamed

"j"Five 3- to 4-day-old female adults were caged for 16 hours on 30-day-old plants. All of the spots produced by feeding on rice plants were white whereas on L. hexandra 80o/0 of the area was dark blue and 20% was white. White spots indicate xylem feeding and blue spots indicate phloem feeding.

E. A. HEINRICHSAND F. G. MEDRANO

83

Survival (%) 100 TNI 80

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lividipennis predation, Anagrus parasitization and B. bassiana infection were highest on the rice N. lugens. Higher L. pseudoannuIata predation on L. hexandra may have been due to the smaller size of the stems and the distribution of the hoppers over the entire plant making it easier to detect the N. lugens prey. L o w e r C. lividipennis predation and Anagrus parasitism on L. hexandra may have resulted from the difficulty of penetrating the hard stem to reach the N. lugens eggs and the difficulty in locating the eggs which were more widely distributed than on T N 1.

D i s c u s s i o n and c o n c l u s i o n s

Leersia hexandra serves as a host for N. lugens. However, the population which occurs on L. hexandra is distinct from that on rice as it does not survive on rice and the rice population does not survive on L. hexandra. Claridge and den Hollander (1982) found that T N 1, which is considered to be a universally susceptible variety, responds to a N. lugens population from rice in Queensland, Australia, as resistant. However, after 10 generations of selection on T N 1 , a population was produced with virulence characteristics allowing it to feed and survive on T N 1, similar to that of biotype 1 at IRRI. In Sri Lanka, local populations o f N . lugens separated by less than I00 km show different virulence patterns and adaptation to the specific rice varieties on which they were collected (Claridge, den Hollander and Furet, 1982). In the case of the Leersia and rice populations on the I R R I farm, it is apparent that distinct sympatric populations occurring in the same area have been selected for feeding behaviour. A survey taken in L u z o n province, Philippines, indicated that N. /ugens populations were c o m m o n on L. hexandra. T h e Leersia population has the potential

N. lugens hosts

84 Predation or parasitism (%)

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I

LH N. lugens

R

80

N. lugens

60

40

1

20

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Predation, parasitism and disease infection in Leersia hexandra (LH) and rice (R) populations of Nilaparvata lugens. Predation by Lycosa pseudoannulata on adults and Cyrtorhinus lividipennis on eggs; parasitism of eggs by Anagrus spp. and nymphs by Pseudogonatopus nudus; and infection of nymphs by Metarrhizium anisopliae and Beauveria bassiana. Asterisks indicate a significant difference between the two N. lugens populations at the 5% (*) and 1% (**) levels. FIGURE 2.

to play an important part in the natural control of N. lugens populations. As the greenhouse studies indicated, the Leersia population can serve as a suitable host for some of the predators , parasites and pathogens that attack the rice population. T h e egg parasite Anagrus sp. was reared from field-collected Leersia hoppers. T h e Leersia population which occurs in moist ditches can serve as an important reservoir for natural enemy populations during the dry season when rice is not available. References AUCLMR,J.L., BALDOS,E. ANDHEINRICHS,E.A. (1982). Biochemical evidence for feeding sites of the leafhopper, Nephotettix virescens within susceptible and resistant rice plants. Insect Science and Its Application 3, 29-34. CHEN,J.M. (1982). Literature Review on Alternative Host Plantsfor the Brown Planthopper, Nilaparvata lugens (StM) including Wild Rice Oryza spp. Los Bafios, Philippines: Entomology Department, IRRI, Mimeo. 32 p. CLARIDGE,M.F. ANDDEN HOLLANDER,J. (1982). Virulence to rice cultivars and selection for virulence in populations of the brown planthopper, Nilaparvata lugens. Entomologia experimentalis et applicata 32, 213-221.

E. A. HEINRICHS AND F. G. MEDRANO

85

CLARIDGE, M.F., DEN HOLLANDER,J. AND FURET, I. (1982). Adaptations of brown planthopper (Nilaparvata lugens) populations to rice varieties in Sri Lanka. Entomologia experimentalis et applicata 32, 222-226. INTERNATIONAL RICE RESEARCH INSTITUTE (IRRI). (1979). Annual Report for 1978. Los Bafios, Philippines: IRRI. 478 p. ELI, HuI-CHI, AND WANG, C.H. (1958). Studies on Nilaparvata lugens (St~l) in Hunan. Acta Entomologica Sinica 1, 283-313 (Chinese with English summary). LEI, HuI-ZHI, LIu, GuI-QuI ANDWU, MEI-Wu (1982). The nymphs of the brown planthopper fed on Leersia hexandra Swartz can grow into adult insects (In Chinese). Kunchon Zhishi 19(1), 48. OKA, I.N. (1979). Cultural control of the brown planthopper, Nilaparvata lugens. In: Brown Planthopper: Threat to riceproduetion in Asia, pp. 357-369. Los Bafios, Philippines: IRRI. 369 p. PAGUIA,P., PATHAK,M.D. ANDHEINRICHS,E.A. (1980). Honeydew excretion measurement techniques for determining differential feeding activity of biotypes of Nilaparvata lugens on rice varieties. Journal of Economic Entomology 73, 35-40. PATHAK,P.K. ANDHEINRICHS,E.A. (1982a). Selection of biotype populations 2 and 3 by exposure to resistant rice varieties. Environmental Entomology 11, 85-90. PATHAK, P.K. AND HEINRICHS, E.A. (1982b). Bromoscresol green indicator for measuring feeding activity of Nilaparvata lugens on rice varieties. Philippine Entomologist 5, 209-212. SHOU, Z.B. ANDGONG, H.S. (1982). A preliminary observation on Nilaparvata lugens (Still) on Leersia hexandra Swartz. (In Chinese). Kunchon Zhishi 19(1), 46-48. Accepted 13 October 1983