Rice white stemborer - Planting synchrony & biocontrol

8/2/2019 Rice white stemborer - Planting synchrony & biocontrol

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Rice white stemborer Scirpophaga innotata (Walker) in southernMindanao, Philippines. II. Synchrony of planting and natural enemies

J. A. LITSINGER 1 , A. L. ALVIOLA 2 , C. G. DELA CRUZ 2 , B. L. CANAPI 3 ,E. H. BATAY-AN III 4 , & A. T. BARRION 2

1 Dixon, CA, USA, 2 International Rice Research Institute, Los Banos, Philippines, 3 Monsanto Philippines, Makati, Metro Manila, Philippines, and 4 Philippine Rice Research Institute, Agusan del Norte, Philippines

AbstractAlthough the rice white stemborer (WSB) Scirpophaga innotata (Walker) has been an epidemic pest in other locations in the

Philippines and Indonesia, its population has remained at chronic pest levels in Koronadal, southern Mindanao, Philippines.Field studies were undertaken to determine the role of egg parasitoids and general predators in suppressing WSB numbers.The results revealed greater mortality levels on WSB than in any other location where benecials have been assessed. Fourhymenopteran parasitoids ( Tetrasticus schoenobii Ferriere [Eulophidae], Telenomus rowani (Gahan) [Scelionidae], Telenomusdignus (Gahan), and Trichogramma japonicum Ashmead [Trichogrammatidae]) combined to parasitise 65% of eggs in thesecond 1990 1991 rice crop. Multiple parasitism occurred in 61% of parasitised egg masses. Egg predation averaged 44%principally by the tettigoniids Conocephalus longipennis (de Haan) and C. maculatus (Leth.). Generalist predators steadily builtup over the rice crop. A contributing factor to the high success of natural enemies could be related to the special situation of two irrigation systems interspersed among each other. Communal systems fed by artesian wells resulted in asynchronousplanting areas where farmers can plant ve crops in 2 years juxtaposed to a larger river diversion system typied by highly synchronous double rice cropping. The heterogeneous habitat created by the two irrigation systems could favour the density-dependent T. schoenobii , the keystone parasitoid in the rice ecosystem, which acts as both a parasitoid and predator.

Keywords: Rice insect pest, ecology, planting synchrony, damage, Scripophaga innotata, S. incertulas, biocontrol,egg parasitoids, predators, multiple parasitism, ecological diversity

1. Introduction

The rice white stemborer (WSB) Scirpophagainnotata (Walker) returned to prominence in theSouthern Philippines and Java in the 1980s where itsupplanted the closely related rice yellow stemborer(YSB) S. incertulas (Walker), probably as a result of itsability to survive El Nino droughts (Litsinger et al.2006). Females of both species lay egg masses mostly on leaf blades, protecting them only with a mat of body hair. Within a day of emergence, stemborer

larvae tunnel into rice tillers where they completedevelopment protected from most natural enemies.Both WSB and YSB share a similar natural enemy complex (Khan et al. 1991) which van der Goot(1925) believed was a signicant mortality factor tocheck stemborer buildup. But van der Goot (1925)noted the reason WSB was a greater pest than YSBwas that in the tropics WSB aestivates, whereas YSBdoes not. By synchronising the eld population of adults, WSB can overwhelm natural enemies in theearly wet season when rainfall terminates diapause enmasse with the result that oviposition becomes highly concentrated, occurring at a time when natural enemy numbers are low. Most studies to determine natural

enemy efcacy of Scirpophaga rice stemborers havebeen done on YSB (Ooi and Shepard 1994).Triwidodo (1993) undertook studies to determinewhy WSB outbreaks occurred in Java upon re-establishment. One reason was insecticide-inducedresurgence. He noted a decline in both egg parasitism(43 21%) and predation (23 13%) when carbo-furan granules were broadcast into the eld as a partof a large scale government subsidised program.

Of WSBs natural enemies, egg parasitoids havebeen the most studied. Van der Goot (1948) recorded

three hymenopterous species (1) Telenomus rowani (Gahan) ( Phanurus beneciens Zehnt.) [Scelioni-dae], (2) Tetrasticus schoenobii Ferriere [Eulophidae]),and (3) Trichogramma japonicum Ashmead [Tricho-grammatidae] causing 65% egg mass parasitism 1 overa 9-year period 1930 1938. More recently Rubia(1994) recorded 90% egg mass parasitism partitionedbetween T. rowani (45%), T. schoenobii (33%), andT. japonicum (22%).

A number of larval and pupal parasitoids have beenrecorded along with predators on WSB but noresearch on efcacy was noted for these guilds(Khan et al. 1991). The only study conducted in thePhilippines on WSB was that by Sison (1929)

Correspondence: J. A. Litsinger, 1365 Jacobs Place, Dixon, CA 95620, USA. Tel: 1 707 678 9068. Fax: 1 707 678 9069. E-mail: [email protected]

International Journal of Pest Management , JanuaryMarch 2006; 52(1): 23 37

ISSN 0967-0874 print/ISSN 1366-5863 online 2006 Taylor & FrancisDOI: 10.1080/09670870600552463


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who noted activity of natural enemies but did notquantify his observations. Insecticides are not sub-sidised in the Philippines but South Cotabato farmerspredominantly use foliar sprays, applying threeapplications per crop but at half the recommended

dosage.Koronadal, South Cotabato was selected as aresearch site because of its noted high pest incidencefavoured by small communal irrigation systems fed by artesian, free-owing wells where all stages of the ricecrop can be noted year round. Interspersed aroundthese areas lies a more recently constructed MarbelRiver Irrigation System (MRIS) managed by thePhilippine National Irrigation Authority. Farmers inthis large river diversion system follow a strict plantingschedule of two rice crops per year. As water delivery occurs at the same time across large command areas,plantings are highly synchronised. In contrast, thecommunal systems have one well per village and far-mers can plant whenever they choose, often plantingve crops in 2 years.

Despite causing severe damage in Java, in Korona-dal WSB damage has been no more than occurredwith YSB (Litsinger et al. 2006). One possible reasonis the contribution of natural enemies which mightalso be favoured by the constant availability of theirhosts. We report on the efcacy of egg parasitoids andgeneralist predators contrasting the results from bothirrigation systems with a view to determine theirpotential role in limiting WSB to chronic pest status.

Larval or pupal parasitoids were not monitored as pastresearch has shown their signicance to be minimal(Rothschild 1970).

2. Materials and methods

Details of the study site and composition of theresearch team were described in the rst part of thisseries (Litsinger et al. 2006).

2.1. Egg parasitoids

One study eld was selected in each of eight farms,four in synchronous and four in asynchronoussystems. The impact of egg parasitoids was deter-mined by individually rearing 25 50 egg massescollected weekly (the number depended on avail-ability) from each 0.2-ha plot untreated withinsecticide per study eld from 1 week after trans-planting (w.a.t.) to 10 days before harvest in thesecond rice crop of 1990 1991. Egg masses cannotbe distinguished between WSB and YSB, but thepercentage of WSB moths collected from light trapsfrom October 1990 to June 1991 highly favouredWSB (99.9%). Fields within each planting area were

staggered over the range of planting dates for eachirrigation system. In the synchronous area thesecond crop occurred October to February whilein the asynchronous area it ran from October to June.

A 10-cm leaf section containing one egg mass wasclipped and held in an inverted disposable plastic vialwith the cut end held by water-saturated tissue paper(Barrion and Litsinger 1985). Both emerging WSBlarvae and parasitoids were counted by species after

eclosion to determine percentage egg mass parasit-ism. Each egg mass was dissected after emergence tonote the presence of dead, fully developed WSBneonate larvae and parasitoids, which when noted,were added to the totals. Nonviable eggs, however,were excluded from counts.

A conversion method was employed to determineboth egg parasitism and egg mass density forScirpophaga egg parasitoids following Catling et al.(1983). They determined each T. schoenobii requiresthree WSB larvae for development, one by parasitismand two by predation. On the other hand, super-parasitism occurs with T. japonicum in which anaverage of two wasps emerge per parasitised egg.Thus the totals for T. schoenobii and T. japonicumwere multiplied by 3 and 0.5, respectively, todetermine egg mortality. The converted egg para-sitoid counts were added to the WSB neonate larvalcounts to derive egg mass size.

Analyses contrasted asynchronous and synchro-nous planting areas with regard to total parasitismand the contribution of each species. Data wereconverted to a weekly basis for analysis for both eggsand egg masses. Parasite emergence was alsocorrelated with egg mass size. As multiple parasitism

(parasitism of an egg mass by more than one species)was common, data were also separated to show thisfrequency in all combinations from one to fourspecies per egg mass.

2.2. Predators

2.2.1. Generalist predator density. The populationdynamics of generalist predators was monitored by motorised suction (D-Vac 1 ) machine and sweep netin the second crop 1990 1991. The suction samplingwas taken individually from 25 hills from the 0.2-haplots in each of the eight study elds on a weekly basisbeginning 2 w.a.t. to 10 days before harvest. Samplelocations were selected randomly along a diagonaltransect across each plot. A mylar plastic tubeenclosure was rst quickly placed around each hill toisolate the sample (Perfect et al. 1983). The collectedarthropods were removed from the D-Vac 1 machineand placed a large plastic bag with a cotton ballsaturated with carbon tetrachloride as a killing agentbefore preservation in vials of 70% alcohol. In addition100 net sweeps were taken from the same elds on aweekly basis for orthopterans and other more mobilepredators. A sweep is a single 180 8 pass with a

pendulum motion of the 38-cm diameter net whilewalking through the foliage. The number of predatorswas recorded after every 10 sweeps by placing thecontents into a large plastic bag. Predators were lateridentied (Barrion and Litsinger 1994) and counted

24 J. A. Litsinger et al.


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with the aid of a stereo-microscope. Predators weregrouped by guild based on taxonomic afnity. Fieldobservations by the team taxonomist (ATB) deter-mined those predators that attacked WSB.

2.2.2. Egg predator efcacy. Predation of egg masseswas quantied using sentinel egg mass exposure(Luck et al. 1988) on the second crop 1990 1991.Eight study elds equally divided among the twoplanting areas were selected. Egg masses wereobtained each week by rst uprooting ve hills of rice per eld and transplanting them in pots. Allarthropods were removed by hand. The hills wereenclosed in a mylar plastic tube cage with meshcovered ventilation windows. Each night 5 10 WSBfemales were placed per cage (collected on walls of buildings with outdoor lights or from the eld) and inthe morning the potted hill of rice was set out in itssame location in the eld. Exposures occurred from2 to 11 w.a.t. The location of each egg mass wasmarked. Hills were examined every 2 days over an8-day period. Missing or partly consumed masseswere considered as preyed upon.

2.3. Stemborer incidence

WSB densities were determined from both thesynchronous and asynchronous planting areas. Mothswere monitored by kerosene light traps (Litsingeret al. 2006) placed one per eight study site from

1 January 1985 to 31 December 1991. Deadheartsand whiteheads were censused on a per-hill basis(n 20 hills per eld) taken in a stratied patternfrom a neighbouring 0.2-ha plot per eld where eggmasses were collected for parasitoid emergence.Mechanical hand counters were used to record thenumber of tillers per hill. Damage was assessedweekly from 2 w.a.t. to 10 days before harvest.Deadhearts and whiteheads were veried by pullingthe tillers to note feeding injury. Data were averagedby each of three growth stages (Yoshida 1981).

2.4. Statistical analysisData were subjected to one-way ANOVA and

regression/correlation analysis where appropriate.Treatment means were separated using the pairedt -test for two variables or least signicant difference(LSD) test for more than two variables. Means areshown with standard errors of the mean (SEM) usinga pooled estimate of error variance.

3. Results


Four egg parasitoids belonging to three familiescombined to parasitise 82% of egg masses and 65%of eggs averaged over the asynchronous and syn-chronous areas during the second crop 1990 1991

(Table I). Parasitised eggs occurred at higher rates inasynchronous areas (71 vs. 60%) averaged over allspecies. T. schoenobii was the most effective parasitoidwhich alone caused 36% egg mortality despiteranking only second highest in egg mass parasitism

(42%). This solitary parasitoid was signicantly moreprevalent in asynchronous planting areas in terms of both parasitised egg masses and eggs.

The phoretic T. rowani was the second mosteffective species parasitising 49% egg masses and17% eggs. It had higher rates of parasitism insynchronous areas in contrast to T. schoenobii .Telenomus dignus (Gahan) followed with equivalentlevels of egg mass parasitism (38%) as T. rowani butparasitised signicantly fewer eggs (6%). It was moreeffective in synchronous areas in terms of eggparasitism but in terms of egg masses there was nodifference of planting area. Both Telenomus speciesare solitary parasitoids. The gregarious trichogram-matid T. japonicum was the least effective species,parasitising 30% of egg masses but only 4% of eggsand was unaffected by planting schedule.

Egg parasitism levels over the course of the cropdiffered for each species. There was no difference inparasitism by crop stage for T. schoenobii , butT. rowani was least prevalent in the ripening stage(Table II). Parasitism levels in the vegetative stagewere highest for T. dignus but least for T. japonicum .Averaging all species, parasitism was least duringripening. Multiple parasitism occurred in 61% of

parasitised egg masses (Table III), averaging 1.5 spe-cies per mass. Equivalent frequencies of egg masseswere parasitised by either one (39%) or two species(38%), but frequency declined with three (20%) orfour (4%) parasitoids per mass. Every possiblecombination of parasitoid species occurred. Fourparasitoid species were recorded in masses as smallas 10 eggs.

Egg parasitism (based only on parasitised eggmasses) was signicantly lowest in single speciescompared to two to four species per egg mass(Figure 1A). Highest egg parasitism rates occurredwith T. schoenobii alone or in combinations. BothT. japonicum and T. rowani occurred more in combi-nations. Highest parasitism levels always occurredwith T. schoenobii regardless of the number of species.But parasitism levels for T. dignus declined drama-tically from single to multiple parasitism. Overallparasitism levels increased with greater multiparasit-ism at the expense of contributions from each species.

A more meaningful measure of efcacy was thedegree to which parasitoids reduced the number of surviving (neonate) WSB larvae per egg mass. Aswith egg parasitism, more than one parasitoid speciesresulted in a greater larval mortality per egg

mass (82 88%) than by single species alone (74%)(Table III). The most effective parasitoid combina-tions (two to nine neonate larvae/mass) again were inT. schoenobii associations. This can be seen bettergraphically (Figure 1B), as T. schoenobii was the most

Rice white stemborer S. innotata in southern Mindanao, Philippines 25


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effective overall in preventing larval emergence,either when occurring singly or with only one moreparasitoid. T. japonicum and T. rowani were not aseffective singly as when they were in combination inreducing larval emergence.

Parasitism rates showed interesting relationshipswith egg mass size. Rates signicantly decreased withincreasing egg mass size from one to 241 eggs permass for T. rowani , T. dignus , and T. japonicumbut not for T. schoenobii which showed no relation-ship (Figure 2A D). The greatest slope wasfor T. rowani . When all species were combined(Figure 2E), the relationship was nullied because of the dominance of T. schoenobii . Larger egg masses(4 58 eggs/mass) also attracted more parasitoidspecies (Table III).

When the data were plotted weekly for bothasynchronous and synchronous planting areas (Oc-tober 1990 to June 1991), egg mass parasitism levelshovered around 100% for the rst 4 months beforedeclining precipitously at the end of each crop(Figure 3A). Egg mass parasitism levels 4 80%occurred for 66 and 67% of the weeks countingboth planting areas. This pattern was repeated foregg parasitism, albeit at lower rates particularly insynchronous planting areas (Figure 3B).

Despite the high parasitism levels for each plantingarea, the data reveal weeks when egg and egg massparasitism rates markedly dipped, unleashing wavesof WSB larvae to attack the crop (Figure 3C). Note

the deepest troughs of Figure 3B match with thepeaks of Figure 3C. These lapses did not necessarily occur in the same weeks for each planting area. Thenumber of larvae emerging averaged 20.0 per eggmass over the whole season but occasionally (lateNovember and in January and February for bothplanting schedules, and repeatedly after March forthe asynchronous area) reached double or triple theaverage.

Egg mass size also uctuated dynamically over theseason ranging from 5 40 to 4 75 eggs in any givenweek (Figure 3D). Larval surges were often asso-ciated with peaks of larger egg mass sizes, particularly when masses averaged 4 60 eggs. There was a strongpositive correlation between increasing egg mass sizeand emerging larval numbers (Figure 4). The line of best t was a quadratic model ( P 5 0.0001, F 57.36, df 20). Focusing on parasitoid speciesfrom the weekly data, T. schoenobii showed generally higher levels of egg mass parasitism for asynchronousthan synchronous areas without an apparent seasonaltrend (Figure 5A). In synchronous areas only,T. rowani (Figure 5B) and T. dignus (Figure 5C)showed similar patterns that closely mirrored that of total parasitism (Figure 5E) where egg mass para-

sitism levels were generally higher and gradually declined with the season. Parasitism levels forT. japonicum (Figure 5D) initially were very low butincreased dramatically at the end of the croppingseason for each planting area.

T a b l e I . W h i t e s t e m b o r e r e g g m a s s a n d e g g p a r a s i t i s m l e v e l s b y f o u r p a r a s i t o i d s p e c i e s i n a s y n c h r o n o u s a n d s y n c h r o n o u s p l a n t i n g

a r e a s , s e c o n d r i c e c r o p , 1

9 9 0

1 9 9 1

, P h i l i p p i n e s .

E g g m a s s e s p a r a s i t i s e d ( % )

E g g s p a r a s i t i s e d ( % )

P l a n t i n g s c h e d u l e

D i f f e r e n c e

2

P l a n t i n g s c h e d u l e

D i f f e r e n c e

2

P a r a s i t o i d

M e a n 1

A s y n c h r o n o u s

S y n c h r o n o u s

P

F

d f

M e a n 1

A s y n c h r o n o u s

S y n c h r o n o u s

P

F

d f

T e t r a s t i c u s s c h o e n o b i i

4 1 . 8

+

3 . 8 a b

5 0 . 6

+

5 . 2 a

3 3 . 3

+

5 . 6 b

0 . 0 2 0

5 . 6 1

6 1

3 6 . 1

+

2 . 4 a

4 7 . 0

+

5 . 7 a

2 5 . 7

+

5 . 5 a

0 . 0 1

7 . 1 4

6 1

T e l e n o m o u s r o w a n i

4 9 . 3

+

3 . 8 a

4 0 . 7

+

5 . 5 a b

5 7 . 4

+

5 . 4 a

0 . 0 4 0

4 . 6 3

6 1

1 7 . 3

+

2 . 3 b

1 2 . 9

+

2 . 9 b

2 1 . 5

+

2 . 8 a

0 . 0 4

4 . 4 7

6 1

T e l e n o m o u s d i g n u s

3 7 . 8

+

3 . 5 a b

3 0 . 3

+

5 . 7 b c

4 5 . 1

+

5 . 6 a b

n s

3 . 4 2

6 1

5 . 6 +

2 . 4 c

3 . 6 +

1 . 2 c

7 . 5 +

1 . 1 b

0 . 0 2

5 . 4 6

6 1

T r i c h o g r a m m a j a p o n i c u m

3 0 . 3

+

3 . 1 b

2 7 . 9

+

4 . 8 c

3 2 . 4

+

4 . 7 b

n s

0 . 4 6

6 1

4 . 1 +

2 . 1 c

3 . 8 +

1 . 0 c

4 . 5 +

0 . 9 b

n s

0 . 2 2

6 1

M e a n

8 2 . 2

8 4 . 6

+

5 . 3

7 9 . 8

+

5 . 2

n s

0 . 9 8 0

6 1

6 5 . 0

7 0 . 5

+

6 . 2

5 9 . 5

+

6 . 0

0 . 0 3

3 . 5 3

6 1

n

2 0 1 6

9 6 0

1 0 5 6

2 0 1 6

9 6 0

1 0 5 6

P

0 . 0 0 6

0 . 0 0 3

0 . 0 0 9

5 0 . 0 0 0 1

5 0 . 0 0 0 1

5 0 . 0 0 0 1

F

4 . 2 6

5 . 0 3

4 . 1 3

3 6 . 5

2

3 5 . 0

1

1 1 . 7

4

d f

1 7 1

1 7 1

1 7 1

1 7 1

1 7 1

1 7 1

1 F i f t y e g g m a s s e s / w e e k f r o m f o u r s i t e s e a c h o f a s y n c h r o n o u s a n d s y n c h r o n o u s p l a n t i n g a r e a s 7 d a y s a f t e r t r a n s p l a n t i n g u n t i l 1 0 d a y s b e f o r e h a r v e s t . I n a c o l u m n , m e a n s

+

S E M

, f o l l o w e d b y a c o m m o n l e t t e r a r e

n o t s i g n i c a n t l y d i f f e r e n t ( P 0 . 0 5 ) b y L S D t e s t . 2

O n e - w a y A N O V A

, c o n d e n c e i n t e r v a l s e t a t P 0 . 0 5

.



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Egg parasitism data followed similar patterns asthat of egg masses for each species (Figure 6A D).The egg parasitism rates uctuated, often dramati-cally, week to week. Notably parasitism rates for allspecies but T. japonicum declined precipitously inmid-November when a surge of larvae was released(Figure 3C), whereas in the prior 2 weeks, rates wereamong the highest. In the asynchronous areas, wherethe second crop occupied a 9-month period, para-sitism declined in February and March for all speciesbut T. schoenobii which made up the difference by being more abundant.

3.2. Predators

3.2.1. Generalist predator density. Three major pre-datory guilds were most abundant in the suctionsampling: (1) spiders, (2) coccinellids, and (3)orthopterans. Spiders preyed on neonate larvae andmoths and included two families which capturepassively by webs: (1) Araneidae [ Araneus inustus(C.L. Koch) and Argiope catenulata (Doleschall)]

and (2) Tetragnathidae [ Tetragnatha maxillosaThorell, T. mandibulata (Walckenaer), T. virescensOkuma, T. javana (Thorell), and Dyschiriognathahawigtenera Barrion & Litsinger]. There were alsofour families of hunting spiders: (1) Linyphiidae

[ Atypena formosana (Oi)], (2) Oxyopidae [ Oxyopes javanus Thorell], (3) Lycosidae [ Pardosa pseudoannu-lata (Boes. et Str.)], and (4) Clubionidae [ Clubiona japonicola (Boes. et Str.)].

Coccinellids also preyed on neonate larvae, com-posed mainly of Coccinella arcuata (F.), Micraspisdiscolor (F.), and Micraspis vincta (Gorham). Ortho-pterans were of two groups: (1) Gryllidae [ Anaxiphalongipennis (Serville) and Metioche vittaticollis (Stal)]which fed on neonate larvae and (2) Tettigoniidae[Conocephalus longipennis (de Haan) and C. maculatus(Leth.)] which fed on neonate larvae and egg masses.The anal tuft matting protects masses from gryllidsbut not from tettigoniids.

Predator density for each of the three guildswas plotted in different sampling units in order tosimplify graphing (Figure 7A). Spiders were the mostnumerous and were the earliest colonisers. Predatorcolonisation by each of the three guilds was initially low but all steadily rose in the late vegetativestage before peaking at the ripening stage. There wereno signicant differences between synchronous and

asynchronous areas in densities of spiders, coccinellids,or orthopterans by paired t -test (Table IV).

3.2.2. Egg predator efcacy. As the majority of thesentinel egg masses were entirely consumed on most

Table II. White stemborer egg parasitism levels for each of four parasitoid species summarised by rice growth stage, second rice crop,1990 1991, Philippines.

Egg parasitism (%) 1

Growth stage T. schoenobii T. rowani T. dignus T. japonicum Total

Vegetative 48.1 + 6.5 a 21.4 + 3.4 a 9.1 + 2.3 a 1.4 + 1.1 b 79.9 + 6.9 aReproductive 34.4 + 7.0 a 21.2 + 3.3 a 5.4 + 1.3 b 6.1 + 1.1 a 67.1 + 6.5 aRipening 26.0 + 7.2 a 9.1 + 3.5 b 2.2 + 1.4 b 4.7 + 0.6 a 45.9 + 6.8 bP ns 0.03 0.004 0.01 0.004 F 2.37 4.17 6.16 4.73 6.40df 61 61 61 61 61

1Emergence from egg masses, n 50 egg masses/week from four sites each of asynchronous and synchronous planting areas from 7 days after

transplanting until 10 days before harvest. In a column, means + SEM, followed by a common letter are not signicantly different ( P 0.05)by LSD test.

Table III. White stemborer (WSB) parasitism summarised by frequency of multiple parasitism, second rice crop, 1990 1991, Philippines.1

Parasitoid species

No. species/mass Frequency (%) Egg parasitism (%) Neonate WSB larvae (no./mass) Egg mass size (no. eggs/mass)

0 51.7 + 2.1 b1 39.3 73.9 + 1.5 b 16.5 + 1.1 b 51.4 + 1.6 b2 37.5 82.6 + 1.8 a 12.4 + 1.1 a 50.3 + 1.6 b3 19.7 82.1 + 2.4 a 13.9 + 1.6 a 58.0 + 2.8 ab4 3.5 87.5 + 5.3 a 12.7 + 3.5 a 68.3 + 5.1 a

4 1 60.7P 5 0.0001 0.04 0.001 F 11.79 3.23 4.46df 1651 1651 2011

1 Fifty egg masses/week from four sites each of asynchronous and synchronous planting areas 7 days after transplanting until 10 days beforeharvest. In a column, means + SEM, followed by a common letter are not signicantly different ( P 0.05) by LSD test.



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occasions, tettigoniids were indicated as the key group. Egg mass predation rose from 10% 2 w.a.t. to4 70% during the ripening stage (Figure 7B).Predation averaged 45% over the 10-week samplingperiod and reected the rise in abundance of orthopterans.

3.3. Stemborer incidence

Light trap collections were averaged for each yearfrom the May to December monthly totals whichrepresented the main rice growing season in thesynchronous planting areas. Moths were 1.7 times

more abundant in the asynchronous areas thansynchronous areas (Table V). Overall stemborerdamage rates, however, were quite low ( 5 3%deadhearts and whiteheads) with no effect of plantingschedule in any of the three rice growth stages.

4. Discussion


The egg parasitoid guild is similar throughoutWSBs range for three core genera ( Tetrasticus ,Telenomus , and Trichogramma ), with species oftendiffering by location. This study is the rst to presentefcacy data for T. dignus on WSB. AlthoughRothschild (1970) and Yasumatsu (1967) questionedT. dignus as a parasitoid of Scirpophaga spp., bothUichanco (1928) and Ishii (1939) reported WSB asa host. T. dignus specimens were compared withmaterial determined by C. R. Baltazar from the

University of the Philippines collection.The 82% egg mass parasitism reported herein is on

par with previous multi-year studies in Indonesia[van der Goot (1948) 72% and Rubia (1994) 4 90%]and Darwin, Australia [Li (1970) 64%]. Fewer

Figure 1. Comparison of the efcacy of each of four egg parasitoid species in terms of (A) egg parasitism and (B) surviving white stemborerlarvae when parasitised by each of four species averaged over synchronous and asynchronous planting areas, second rice crop, 1990 1991,Koronadal. T. sch Tetrastichus schoenobii , T. row Telenomus rowani , T. dig Telenomus dignus , T. jap Trichogramma japonicum .



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Figure 2. Regression analyses showing the relationship between egg parasitism and egg mass size for (A) T. schoenobii , (B) T. rowani , (C) T.

japonicum , (D) T. dignus , and (E) all four parasitoids, averaged over synchronous and asynchronous planting areas, second rice crop, 1990 1991, Philippines.



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studies have measured WSB egg parasitism. Van derGoot (1948) did not present his data as percentage of eggs parasitised but, based on his reported meannumber of neonate WSB larvae/egg mass and mean

of 81 eggs per egg mass, egg parasitism wascalculated to be 33%. Learmonth (1981) in theOrd River Valley, Australia, recorded 48% eggparasitism dominated by T. rowani over 3 years inthe only other seasonal study found. Thus the

Koronadal rate of 65% egg parasitism is 86 and35% higher than each of these two studies.

In terms of the relative abundance of each specieswithin a guild, van der Goot (1948) recovered more

T. rowani (73%) than T. japonicum (25%) and leastwith T. schoenobii (2%) from parasitised eggs. Morerecently in Java, Rubia (1994) also found T. rowani headed the list but was not as dominant (45%eggs parasitised), with more contributions from

Figure 3. Effect of egg parasitoids on white stemborer in synchronous and asynchronous planting areas on parasitism of (A) egg masses and(B) eggs, and on (C) surviving larvae in relationship to (D) egg mass size, second rice crop, 1990 1991, Philippines. Synchronous sites wereharvested in February and asynchronous sites in June.



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T. schoenobii (33%) and T. japonicum (22%). Li(1970) arrived at the same ranking with T. rowani ,

Tetrasticus ( Aprostocetus ) sp., and T. japonicum .A similar ranking occurred in Koronadal in terms of egg mass parasitism in which T. dignus was thirdmost prevalent (Table I). But in terms of eggparasitism, T. schoenobii was responsible for 36% of egg mortality and thus the most important parasitoidin Koronadal.

From the stacking of layers of eggs in an eggmass, the more exposed outer layers protect theinnermost ones from direct parasitism as the centremay be up to four layers thick. Based on geometry, asthe size of an egg mass increases, more inner eggs areprotected and thus egg parasitism decreases propor-tionally for all non-phoretic species. Masses 4 100eggs registered 5 50% egg parasitism on average duenot only to the greater protection afforded to theinnermost eggs but also that a parasitoid female (of any of the species) has, at any one time, a maximumcomplement of only 30 40 eggs (Rothschild 1970).

T. schoenobii was considered the most effectiveparasitoid in the study based on the following vecharacteristics: (1) being specic to Scirpophaga spp.,(2) being density dependent (Catling et al. 1983) (itresponds to rising WSB egg densities; evidence fordensity dependence was its greater prevalence in

the more WSB-dense asynchronous sites), (3) beingequally active in all crop growth stages, (4) being thelargest species it has the longest ovipositor and thusmost able to penetrate the protective matting; it caneven oviposit through the leaf blade from below to

reach the lowest tier (Rothschild 1970), and (5) oncea mass is found it has an advantage due to its

additional predatory ability for the progeny of onefemale to destroy over 100 eggs.The two Telenomus species were more prevalent

in the less populous synchronous areas thus wereconsistent with Catlings (1979) nding of theirbeing density independent. The phoretic behaviourof T. rowani provided an advantage in locating eggsover T. schoenobii as all eggs have an equal chance of being parasitised regardless of location in a mass.There is no evidence that T. dignus exhibits phoresy,but it parasitises a wider host range, mainly Chilo spp.Both Telenomus species, and T. dignus in particular,are known to be poor searchers in the later growthstages probably as result of a denser canopy (Shepardand Arida 1986). T. rowani , however, makes upfor poor searching for egg masses by its phoreticbehaviour.

T. japonicum was the least effective parasitoid interms of percentage of egg parasitism due to dilutionfrom superparasitism. Being the smallest, its shortovipositor can only reach the most exposed eggs. Butdespite its small size, T. japonicum appeared to beable to search older and more dense canopiesrelatively better than Telenomus spp.

Multiple parasitism, common with YSB as

well (Catling et al. 1983; Kim et al. 1986), is anatural outcome of large parasitoid complexes(Catling 1979). Multiple parasitism by members of ones own species is less likely due to species-specic chemical cues (Danyk and Mackauer

Figure 4. Relationship between egg mass size and the number of surviving larvae as a result of egg mass parasitism, average of synchronousand asynchronous areas, second rice crop, 1990 1991, Philippines.



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Figure 5. Weekly egg mass parasitism of the white stemborer by four parasitoids averaged over four elds each in synchronous and

asynchronous planting areas, second rice crop, 1990 1991, Philippines. Synchronous sites were harvested in February and asynchronoussites in June. Labelling of months centred on mid-month.



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1993). They noted that with few exceptions,different parasitoid species do not recognise oneanothers cues. Evidence of multiple parasitism by

conspecics was revealed in the current study by theobservation of groups of individuals of the samespecies emerging at different times in the same

Figure 6. Egg parasitism of the white stemborer by four parasitoids averaged over four elds each in synchronous and asynchronous plantingareas, second rice crop, 1990 1991, Philippines. Labelling of months centred on mid-month.



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mass, a phenomenon also observed by Islam (1976)

in YSB. There was evidence that multiple parasitismby different species had higher rates than asingle species including multiple parasitism of conspecics. It was commonly observed, that inmultiple parasitised egg masses, only 5 5 wasps

emerged for a given species which is far fewer than

would be the case if the mass were parasitised by asingle female.

Due to the high level of multiple parasitismobserved in egg masses, superparasitism (aside fromT. japonicum of self) must be common between

Figure 7. Time series of (A) densities of selected predator guilds sampled by D-Vac 1 suction machine averaged over eight elds each of 12crops in synchronous and asynchronous areas, 1985 1991, and (B) egg mass predation rates against the white stemborer determined by thesentinel egg mass method in the second rice crop, 1990 1991, Philippines.

Table IV. Comparison of seasonal densities of three predator guilds in synchronous and asynchronous planting areas in double cropped rice,1985 1990, Philippines.

Planting schedule 1 (no./25 hills/week)

Predatory guild Synchronous Asynchronous P F df

Spiders 0.89 + 0.25 2.52 + 15.8 0.078 ns 1.13 12Coccinellids 0.047 + 0.003 0.95 + 0.18 0.172 ns 1.78 12Orthopterans 0.48 + 0.37 0.47 + 0.18 0.484 ns 0.98 12

1 Annual mean + SEM, DVac 1 suction samples taken weekly over a 6-year period from 25 hills 2 w.a.t. to 10 days before harvest in each of four elds in synchronous and asynchronous planting schedules, P 0.05.

Table V. Comparison of white stemborer incidence in synchronous and asynchronous planting schedules, 1985 1991, Philippines. 1

Stemborer damage by growth stage (%) (deadhearts and whiteheads)3

Planting schedule Annual light trap collection (no./mo.) 2 Vegetative Reproductive Ripening

Synchronous 248.4 + 53.7 1.89 + 0.44 1.84 + 0.27 1.70 + 0.48Asynchronous 432.7 + 64.9 1.47 + 0.23 1.30 + 0.31 2.76 + 0.57P 0.037 * 0.382 ns 0.173 ns 0.137 ns F 5.51 0.788 1.951 2.357df 12 28 28 28

1Means + SEM, condence interval P 0.05, by paired t -test.

2Average of daily collections summed by month from May to December

during the main growing season, two traps in each of two villages per planting schedule. 3 Weekly samples from 20 hills in four elds perplanting schedule taken from 2 weeks after transplanting to 10 days before harvest.



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species, particularly among the most vulnerableoutermost eggs. In addition T. schoenobii s predatory larvae undoubtedly do not discriminate betweenparasitised and nonparasitised eggs. Despite theintraspecic and interspecic competition, multiple

parasitism and superparasitism are considered bene-cial and a necessary outcome to cope with large eggmasses that can only be successfully parasitisedduring a very narrow window of time (before thethird day after egg mass deposition) (Bhuiyan andSuan 1986). Even in times of apparent parasi-toid abundance, Catling et al. (1983) observed thatYSB parasitism levels periodically became depressed,going from several weeks of 50 60% parasitism toone or 2 weeks at 5 20%. These brief periodsthat unleashed high numbers of stemborer larvaewere also noted in this study, often coinciding withperiods of increased egg mass size (Figure 1).Thus factors which contribute to larger egg massessuch as improved nutrition from crops receivinghigh rates of inorganic N fertiliser (Litsinger 1994)would indirectly increase WSB damage.

4.2. Egg predators

Orthoptera (gryllids and tettigoniids), Odonata(libellulids and coenagrionids), Coleoptera (coccinel-lids, carabids, and staphylinids), aquatic Hemiptera,and Araneae are reported as the principal predatory guilds of eggs, larvae, and adults of Scirpophaga spp.

(Rothschild 1971; Ooi and Shepard 1994; Catlingand Islam 1995). Pupae by being inside tillers are outof reach to most predators.

The moth scale matting covering protects eggmasses against all predators but tettigoniids, cara-bids, and staphylinids. Of these three families, thelarge tettigoniids can consume one to two masses perday (including matting) (Rubia et al. 1990). Evi-dence presented showed Conocephalus longipennis andC. maculatus most likely were responsible for the highpredation rates in Koronadal. These predators t theobservations of (1) consuming the whole mass thusleaving no trace and (2) increased abundance in thelate growth stages. Pantua and Litsinger (1984) andShepard and Arida (1986) reported similar resultsagainst YSB. Conocephalus is particularly attractedto late stage rice as it also feeds on owers andspikelets (Barrion and Litsinger 1987). Its role as aneffective predator overcomes this negative role asmodern rices set many more spikelets than can belled.

A larger array of predators feed on neonate larvaebefore penetrating tillers. Older WSB larvae exit andenter new tillers up to three times, particularly on ayounger crop (Rubia et al. 1997) becoming vulner-

able to predators. These include spiders whichCatling and Islam (1995) felt were the most impor-tant predatory guild overall against stemborersbecause of their numerical dominance, populationstability, and diversity of species. Suction sampling

veried their high densities and presence throughoutthe crop cycle supporting this statement. Coenagrio-nid adults y within the foliage to pick off larvae(Litsinger et al. 1997). Coccinellid larvae and adultshunt for larvae on the foliage (Ooi and Shepard

1994). Their numbers also increased late in theseason (Figure 7A) as pollen from spikelets is afavoured food. The early orthopteran abundance inKoronadal was traced to Metioche vittaticollis and Anaxipha longipennis that targeted larvae (Rubia andShepard 1987).

The key groups that prey on Scirpophaga mothsare Odonata and most species of riceeld spiders(Yasumatsu et al. 1975). Adult predators play akey role and complement egg parasitoids well. Thevery low insecticide dosages employed by Koronadalfarmers may be the reason natural enemies are spareddespite the high application frequencies.

4.3. Pest status and the role of asynchronous planting

Studies of natural enemies provided evidence thatWSB is under heavy suppressive pressure throughoutthe crop. Egg parasitoid activity in Koronadalresulted in the highest mean egg mortality comparedto Java (van der Goot 1948) or Australia (Learmonth1981). The higher rates of egg parasitism in asyn-chronous areas must be a key factor in reducingWSB to chronic pest status in Koronadal in contrast

with Java and northern Mindanao. Thus despite 1.7times greater moth density in the asynchronousareas, damage was no higher than in the synchronousareas attesting to the responsiveness of naturalenemies. The key parasitoid in Koronadal amongfour species was T. schoenobii in contrast to the Javaor Australian studies where T. rowani dominated.Generalist predatory densities built up rapidly in thecrop resulting in a mean predation rate of 44% inKoronadal that complemented the periods when eggparasitism was low.

The juxtaposition of synchronous and asynchro-nous areas among each other augmented theavailability of rice elds in all stages of developmentyear round. The fact that the communal systems areinterspersed throughout the river-diversion, synchro-nised system, meant that natural enemies coulddisperse between them. This favoured T. schoenobii which was the only egg parasitoid signicantly moreabundant in the asynchronous area. Egg predatorswere equally abundant in both irrigation systems.The minimal damage by WSB in Koronadal can beattributed at least in part to the role of naturalenemies and this study supports Way and Heong(1994) and Settle et al. (1996) who argue that

cropping systems should be designed with suchhabitat heterogeneity and biodiversity for this pur-pose as synchronous planting suffers from too fewnatural enemies early in the season due to highmortalities over the fallow period.



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Note1 Note the distinction between egg mass parasitismand egg parasitism. Also parasitism includes thecontribution of predation from T. schoenobii which

plays both roles but is considered a parasitoid.

Acknowledgements

The able assistance of the Koronadal site staff Beatriz Datijan, Anita Labarinto, Hector Corpuz, and Joseph Siazon is gratefully acknowledged. The work of J.H. Lourens in translating van der Goots 1925treatise from Old Dutch to English was a key tounderstanding WSB ecology. Thanks also go to thePhilippine National Irrigation Administration staff inKoronadal for providing the rainfall data as well as thestaff in the Philippine Department of AgricultureRegion XI and XII ofces in Davao and Koronadalfor supporting the project. The kind assistance of Dale Bottrell of the University of Maryland inproviding literature sources is much appreciated.

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