International Journal of Pest Management Vol. 57, No.

2, April-June 2011, 117131

Eect of multiple infestations from insect pests and other stresses to irrigated rice in the Philippines: II. Damage and yield loss
J.A. Litsingera*, J.P. Bandongb and B.L. Canapib
a

1365 Jacobs Place, Dixon, CA 95620, USA; bInternational Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines

(Received 5 March 2010; nal version received 5 October 2010) Single and multiple species infestations of common insect pests were compared in terms of yield loss involving crop stresses that included weeds, sheath blight (Rhizoctonia solani Kunh.), drought, and deciencies of N and solar radiation in addition to insect pest infestations. Losses from the various combinations of stresses were found to be additive, antagonistic, or synergistic. Most combinations of insect pests produced additive losses, with the balance being antagonistic, so implying that compensation occurred. Combinations of insect damage with other biotic and abiotic stresses produced mostly synergistic crop losses, which were signicantly greater than additive ones. Among insect pests, additive losses resulted from yellow stemborer (Scirpophaga incertulas [Walker]) attacking two rice growth stages while the same was true for leaolder (Cnaphalocrocis medinalis [Guenee]). Only the combination of whorl maggot (Hydrellia philippina Ferino) and defoliators (a mixture of Naranga aenescens Moore and Rivula atimeta [Swinhoe]) produced synergistic losses. Knowing the mode of yield loss from combinations of dierent plant stresses will aid the farmer in making decisions regarding which ones should be corrected and which the crop can tolerate. Keywords: rice insect pests; yield loss; multiple pest infestation; drought stress; nitrogen stress; weeds; sheath blight disease; articial pest infestation; damage compensation; green manure; solar radiation

1.

Introduction

Three separate studies in the Philippines have shown that, for a given rice growing community, there normally exists extreme yield variation (19 t/ha) in a given season between even adjacent elds in tropical wetland rice culture (Litsinger 2009). The conclusion from those studies was that some farmers are better managers than others (Pingali et al. 1990). However, Litsinger (2009) showed that even the same farmer could experience such a magnitude of yield variation over consecutive years due to crops being compromised by dierent mixes of plant physiological stresses, including insect pest injury, from season to season. Losses can be high from stresses whose management lies outside of the farmers capacity to correct, even though he may be highly trained and knowledgeable. Losses are rarely the result of only a single pest or a stress acting in isolation thus, more attention needs to be paid to rice injury proles that result from the collective eect of the many stresses acting upon a crop in a given season. Recent studies concluded that the degree of yield loss caused by a given insect pest complex in a eld depends signicantly not only on pest numbers but also on their interaction with the rice production environment (Willocquet et al. 2000). Some of the environmental factors may increase crop compensation, others may exacerbate loss, while others

may be neutral. Higgins et al. (1983) remarked that if joint inuence of two types of pests is synergistic rather than being simply additive, then recommendations developed for single pests might fail. They also mentioned that there is often limited data to quantify the crops response to such interactions. Johnson (1987) emphasised that undertaking research on multiple pest infestations aims to understand how combined pest infestations interact to aect yield. One purpose of our study is to examine how such interactions can aect pest management decisionmaking. For any one pest, a variety of factors can aect the yield loss relationship: the growth stage attacked, intensity of injury, the duration of the attack, and environmental factors aecting plant and crop growth (Bardner and Fletcher 1974). Poston et al. (1983) and Lamp et al. (1985) categorised the mode of interactions from multiple pest infestations as being: (1) additive (no interaction) where yield reductions caused by more than one pest attacking one plant are the sum of the reductions as if each species attacked separate plants, (2) synergistic where the response is signicantly more than additive, and (3) antagonistic where the interaction is signicantly less than additive. In E.A. Heinrichs pioneering research that compared multiple infestations of common rice insect pests, he showed there were synergistic relationships over two seasons where combinations of pests caused much

*Corresponding author. Email: jlitsinger@thegrid.net

ISSN 0967-0874 print/ISSN 1366-5863 online 2011 Taylor & Francis DOI: 10.1080/09670874.2010.537792 http://www.informaworld.com

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J.A. Litsinger et al. Management practices of the trials were those typical of the best farmers in the sites who had adopted modern rices. Trials involved IR64, a modern rice developed at the International Rice Research Institute (IRRI) in Los Banos, Philippines with a maturity of 112 days. IR64 is resistant to brown planthopper (Nilaparvata lugens Stal) and green leafhopper (Nephotettix virescens Distant) and is moderately resistant to stemborers, but susceptible to whorl maggot, defoliators, and leaolder. Transplanting was done with 30-day-old seedlings grown in wet seedbeds at 68 seedlings per hill and 20620 cm spacing between hills in Zaragoza and 25625 cm in Guimba. Unless otherwise stated, N was applied at 40 kg/ha basal and top-dressed with another 40 kg/ha 7 days before panicle initiation. Also 30 kg P and 30 kg K/ha were applied basally. Yields, unless otherwise specied, were taken from 25-m2 samples with the grain weight adjusted to 14% moisture. 2.2. Field trials

higher losses than the sum of the component species infested separately. In the wet season trial, the comparison was 11% yield loss from three pests infested separately vs. 24% loss when infested together (IRRI 1983) and in the dry season trial it was 21% when infested separately vs. 59% loss when infested together (IRRI 1984). We expand on Heinrichs trials and compare yield losses from infestations of multiple pest species both in the same or dierent crop growth stages, as well as infestations combined with other biotic stresses: weeds or sheath blight (Rhizoctonia solani Kunh). In addition, insect infestations are combined with abiotic stresses such as N deciency, drought, and/or reduced solar radiation. The main objective was to determine which combinations of stresses produced the greatest losses and to determine the mode of loss for each. Litsinger (1991) hypothesised that synergistic losses would occur from several pests simultaneously acting on the same crop growth, particularly if the stresses aected dierent crop physiological pathways. The same pest aecting more than one growth stage, such as stemborers or leaolders, should produce an additive response. It is anticipated that such knowledge would identify new strategies for insect pest management and elucidate causation for the inexplicable high yield losses that are sometimes ascended with low pest densities (Litsinger 2009) and why yields vary so widely within a farm community. Field trials involved three chronic insect pest guilds: whorl maggot) Hydrellia philippina Ferino) and defoliating caterpillars that we term defoliators (green semi-looper, Naranga aenescens Moore, and green hairy caterpillar, Rivula atimeta [Swinhoe]) that infest a young crop, and also two pests which attack multiple crop stages: yellow stemborer (Scirpophaga incertulas [Walker]) and leaolder (Cnaphalocrocis medinalis [Guenee]). This is the second part of a two-part study on the eect of multiple pest and stress on yield. The rst part deals with the derivation of damage functions (Litsinger et al. 2011).

Insect pest infestations were articially manipulated to be at or just below their action threshold levels. The stresses imposed in the articial infestations were meant to be moderate in severity, not unlike those commonly found in some elds during each cropping season. Fields were sown early, to escape natural pest infestations. 2.2.1. Combination of whorl maggot and defoliator infestation under dierent N sources on yield A wet season trial was established in Guimba to compare the yield response of a rice crop provided with either organic or inorganic sources of N combined with four articially infested insect pest treatments. Organic N was derived from growing Sesbania rostrata Bremek. & Oberm, a green manure crop, established from 30 kg seed/ha without applied inorganic N. The second complement of treatments received urea (80 kg N/ ha). The four insect infestation treatments were: (1) whorl maggot, (2) defoliators composed of mixed populations of Rivula and Naranga, (3) both whorl maggot and defoliators, and (4) uninfested. Articial insect infestation was carried out in nylon-mesh wooden-frame screen cages set over each plot on the day of infestation. Infestation occurred 3 days after transplanting: (1) 100 whorl maggot adults per plot swept from elds at IRRI and (2) 100 mixed Naranga and Rivula moths per plot obtained from a rearing colony at IRRI. Cages prevented egg predation and were removed 10 days later to minimise the eect of shading on crop yield (Simmons and Yeargan 1990). The randomised complete block design experiment of eight treatments was replicated three times in the 50m2 plots. Shallow bunds were constructed around each plot to prevent inter-plot oodwater movement. Land

2. 2.1.

Materials and methods Site descriptions and general crop management

Field trials were carried out in two irrigation systems in Nueva Ecija province, each staed with a dierent research team. Zaragoza is located at the tail end of the Upper Pampanga River Irrigation System in the countrys largest rice bowl. Guimba lies at the edge of that rice bowl, adjacent to rainfed wetland rice areas, and is irrigated by ground water lifted by electric pumps servicing command areas of about 100 ha each. The rainfall pattern in both sites is monsoonal, essentially cloud- and rain-free in the dry season. Further site descriptions can be found in Litsinger et al. (2005).

International Journal of Pest Management preparation was the same in all plots and the green manure crop was allowed to grow for 45 days before being ploughed 1 month prior to the elds being prepared for the rice crop. The amount of N provided from Sesbania was estimated to be 98 kg/ha as determined by the Kjeldahl method in the IRRI Analytical Laboratory. Seedlings were transplanted the same date in all plots. 2.2.2. Combination of defoliator, stemborer, and leaolder infestation on yield A second eld trial was set up at Guimba in the dry season to measure the eect of combinations of three common chronic insect pests on yield. The trial, a randomised complete block design of 12 treatments, each replicated three times in 25-m2 plots, was articially infested with three insect pest guilds. Defoliators were a mixture of third to fourth instar Naranga and Rivula larvae infested at 4 larvae (2 larvae per species)/hill 3 weeks after transplanting (WT). Leaolder was infested at 5 WT at the same larval density and stages as for defoliators. Yellow stemborer was infested at 3 medium sized egg masses/m2 (cut to a standard size by a razor) at 3 WT for deadhearts or 6 WT for whiteheads following the method of Bandong and Litsinger (2005). Caging only occurred for 1 week in the articial infestation of stemborer to allow neonate larvae time to penetrate tillers in a predatorfree environment. All insects were obtained from rearing colonies at IRRI. Four treatments of individual pest injuries formed the basis of comparisons: (1) defoliators, (2) leaolder, (3) stemborer deadhearts, and (4) stemborer whiteheads. There were four additional treatments where two dierent selected pests were combined as well as two more treatments involving a combination of three dierent pest injuries. Lastly, there was the combination of four pest injuries as well as an uninfested check making a total of 12 treatments. 2.2.3. Stemborer damage combined with a weed, a pathogen, and/or drought stress on yield An articially-manipulated, small-plot trial conducted at Guimba tested stemborer whitehead damage combined with drought stress, sheath blight pathogen, and/ or a common grassy weed Echinochloa glabrescens Munroe ex Hook f. Plot size in the randomised complete block design was 16 m2 with four replicates. All plots, except the drought stress treatment, were continually ooded to a depth of 25 cm until 10 days before harvest when the eld was then drained. In the drought treatment, there were two periods of stress in the dry season trial. The rst was during the late reproductive stage when the soil was allowed to dry until the heavy clay soil cracked and leaves began to roll. In irrigated rice, roots are shallow, mostly

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occurring above the natural plow pan. Drying lasted 1 week before irrigation was resumed until a second drought stress period was inicted during the ripening stage, also for 1 week. Echinochloa seedlings were grown in a wooden planters box containing soil that served as a seedbed. One-week-old Echinochloa seedlings were transplanted 2 WT evenly in each plot at 10 plants/m2. Other emerging weeds were hand removed during the rst month of the trial. The weed canopy eventually rose above that of the rice crop further stressing the crop by shading. The percentage of ground covered and the percentage area covered above the canopy by the weed were assessed following Savary et al. (1994). Sheath blight was induced with sclerotia obtained from IRRI cultures and inoculated at 200 mg per hill at 6 WT. Sheath blight was assessed both by the percentage of tillers infected and the estimated percentage of tiller area infected. Stemborer was infested with 48 standardised, medium-sized egg masses per plot spread equidistantly at 3 WT for deadhearts and 6 WT for whiteheads following the method of Bandong and Litsinger (2005). A yield cut was taken from a 10-m2 area. 2.2.4. Insect pest infestations with and without weed stress at four N rates in two seasons Two sets of articial infestation trials in both a wet and dry season crop were conducted in Zaragoza with the objective to derive damage-yield loss functions as reported in the companion paper (Litsinger et al. 2011). The yield data are included in this paper, which is a better arena for discussion of the eect of multiple pest infestation alone and when combined with selected biotic and abiotic variables. The insect pests were whorl maggot and defoliators acting separately and in combination as well as stemborer or leaolder attacking one or both rice growth stages (reproductive and ripening stages). The crop was further stressed from weed competition N deciency, and/or solar radiation deciency (wet season vs. dry season). For simplicity only the 0 and 90 kg N/ha rates were included for analysis. Data on the mean daily level of solar radiation was measured in an agro-met station by an actinograph set up in nearby Guimba for both seasons. Resources did not allow the conduct of a second year of trials that would have replicated each season, but the eect of solar radiation on rice crop growth has been shown to be highly signicant (Yoshida 1981) that we include it as part of the discussion. While humidity and the number of storms also dier between seasons and could contribute to dierences in crop response, solar radiation has been shown to be the most important physical factor aecting crop growth between the two seasons. The early planting that took place to escape natural pest infestations minimised these two

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J.A. Litsinger et al. condent that Rivula and Naranga caused similar injury equivalents as they attack the same growth stage. Whorl maggot, however, makes a dierent injury causing leaf distortion, as the larvae are internal feeders of young meristems. Articial infestation of whorl maggot and defoliators fell within the same range of percentage damaged leaves, thus damage levels were statistically analysed together to compare both N sources. There was no dierence in leaf damage between N source for either pest guild, whether articially infested as a single species (15.124.7% damaged leaves columns A and C) or from the contribution of each species from combined infestations (14.323.4% columns B and D) (Table 1). For each source of N and each pest, infestation was additive in terms of damaged leaves attributable to each species (34.344.1%) or in combined infestation (36.443.4%). Thus the damage from the combined infestation equalled the sum of the damage from whorl maggot and defoliators infested individually. Also the portion of the damage in the combined infestation attributable to whorl maggot was equal to that of the damage level when whorl maggot was infested singly with the same being true for defoliators. Thus in Table 1 the columns were additive: A C B D. The results were similar in both inorganic N or green manure treatments. Yield, however, was signicantly higher in the green manure treatment (4.42 t/ha) than in the inorganic N (4.14 t/ha) in the uninfested as well as in the three infested comparisons (Table 2): whorl maggot (3.85 vs. 4.31 t/ha), defoliators (4.11 vs. 4.54 t/ha), and combined (3.42 vs. 4.03 t/ha). Within each source of N, yields were signicantly lower in the combinations compared to each pest infested singly. The resultant yield loss gures showed there was no loss when defoliators were the only pest guild in either N treatment (0.1 and 72.7%). With whorl maggot, however, there was a signicant loss only in the inorganic N treatment (7.0%) vs. 2.5% with Sesbania. Yield loss was signicantly highest in the combined

variables as storms tend to occur later in the wet season. Each treatment consisted of 150 hills that covered a wide range of infestation levels per pest. Yield was taken on a per-hill basis. Percentage yield loss was calculated for each pest by subtracting the mean yield of damaged hills from that of the undamaged hills divided by the undamaged hills multiplied by 100. 2.3. Statistical analysis

All statistical analyses were performed by SAS with P  0.05 as the criterion for signicance. Results were subjected to one-way ANOVA, and regression analyses were performed where appropriate. Regression models of best t were conducted using SAS software. Treatment means were separated using the paired ttest for two variables or Least Signicant Dierence (LSD) test for more than two variables. Means are shown with standard errors of the mean (SEM) using a pooled estimate of error variance. 3. Results

3.1. Combination of whorl maggot and defoliator infestation 3.1.1. Dierent N sources Natural infestation by either whorl maggot or Rivula and Naranga defoliators attained 53% damaged leaves, thus early planting was successful in minimising this potential bias in the Guimba wet season eld trial. Leaves that showed damage from both whorl maggot and defoliators were counted separately, as the injury for each is distinct. Defoliators either cut holes in the leaves or scrape surface tissue. Hutchins et al. (1988) found in soybeans that each of ve defoliator species comprising two insect orders that attacked the same stage of soybean caused identical physiological responses that they termed injury equivalents as defoliation for each species was deemed similar in its eect on the plant. Based on this result, we feel

Table 1. Damage from rice whorl maggot and Rivula and Naranga defoliators articially infested as individual species or combined on IR64 rice grown under two sources of N, Guimba, Nueva Ecija, Philippines, 1990 wet season. Damaged leaves (% at 35 d after transplanting)2 Whorl maggot (Wm) N kg/ha 80 98 Infested separately (A) 15.1+7.1 a 24.7+9.8 a In the combination (B) 23.4+4.9 a 21.3+6.1 a Defoliator (Def) Infested separately (C) 19.2+8.7 a 19.4+11.2 a In the combination (D) 20.1+5.6 a 14.3+5.0 a Wm Def3 Infested separately (AC) 34.3+11.3 b 44.1+13.5 b Combined infestation (BD) 43.4+12.9 b 36.4+12.2 b

N source1 Urea S. rostrata

1 2

Sesbania green manure legume was plowed under 45 d after sowing providing 98 kg N/ha while urea supplied 80 kg N/ha. 100 whorl maggot adults or 100 Rivula or Naranga moths were infested per 25 m2 3 d after transplanting and caged for 10 days. Within all columns regardless of pest species or combination, means+SEM, followed by a dierent letter are signicantly dierent (P  0.05) by LSD test. The randomised complete block design experiment of eight treatments was replicated three times. 3 The same leaf could be counted twice, once for each pest if damaged by both.

International Journal of Pest Management

Note: 1Sesbania green manure legume plowed under at 45 d after sowing providing 98 kg N/ha while urea supplied 80 kg N/ha; 2Means+SEM within the four uninfested and infested columns followed by a dierent letter are signicantly dierent (P  0.05) by LSD test; 3Means+SEM within the three yield loss columns followed by a dierent letter are signicantly dierent (P  0.05) by LSD test. Yield loss is measured as the dierence in yield between the uninfested and each of the three infested plots for each N source.

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Table 2. Yield loss from rice whorl maggot (Wm) and Rivula and Naranga defoliators (Def) articially infested as individual species or combined on IR64 rice grown under two sources of N, Guimba, Nueva Ecija, Philippines, 1990 wet season.

17.4 8.8

Wm Def

infestations than when infested singly, more so with urea (17.4% loss) than the green manure treatment (8.8% loss). 3.1.2. Damage function trial

0.72+0.23 c 0.39+0.18 b

t/ha

Infested plots

4.11+0.29 bc 4.54+0.42 a

Defoliators

Summarising only the data for whorl maggot and defoliators in the damage function trial allowed an independent comparison over two seasons that contrasted the damage from both pests singly with combined infestations. Damage levels were similar allowing statistical comparisons to be made between all species. In the wet season, injury from whorl maggot and defoliators infested individually was not statistically dierent from each other (31.7 and 34.8% damaged leaves) nor from that of the combined infestation (49.3%), but was statistically dierent when the injury was summed (66.6%), indicating an antagonistic relationship when combined (Table 3). Yield loss, however, indicated a synergistic response, as the losses from each pest (74.5 and 4.6%) were statistically dierent from the combined infestation (27.0%), whereas the sum of the individual infestations was not signicantly dierent from each pest individually (0.1%). In the dry season, damage from whorl maggot and defoliators infested individually resulted in similar levels ranging from 20.7 to 24.7% damaged leaves. When the individual infestation densities were summed, the resultant 45.4% damaged leaves was similar to that in the combined infestation (40.9%). The multiple pest damage therefore was additive. But with yield loss, the sum from individual infestations (17.8%) was statistically dierent than when infested individually (6.1 and 11.7%), but when both insects were infested together the loss was 29.6%, signicantly higher than the sum, indicating a synergistic eect. 3.2. Combination of stemborer damage in two growth stages Yield losses from the Zaragoza wet season damage function trials, where rice hills were articially infested with stemborer eggs in either the reproductive or ripening stages or both stages combined, provided a comparison of single-stage and combined-stage damage. Damage levels from infestation in either the reproductive (18.5% deadhearts whiteheads) or ripening (17.7%) stages were half of that when they were infested together (42.7%). This total was statistically equivalent to the sum of each (36.2%), revealing an additive eect (Table 4). Yield loss, in contrast to whorl maggot and defoliators, was also additive. When infested in only one stage, the loss was 18.8 and 22.4%, which was signicantly less than loss from infestation at both stages (37.2%). The sum of the individual losses (41.2%) was statistically equal to the combined infestation, again indicating additivity.

Yield loss3

Defoliators

Whorl maggot

Yield (t/ha)2

Whorl maggot Uninfected N source

1

Urea S. rostrata

4.14+0.26 bc 4.42+0.32 a

3.85+0.19 c 4.31+0.28 ab

3.42+0.16 d 4.03+0.25 c

Wm Def

0.29+0.10 b 0.11+0.08 a

t/ha

7.0 2.5

0.03+0.09 a 0.12+0.08 a

t/ha

0.1 2.7

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J.A. Litsinger et al.

Table 3. Comparison of the level of damage and yield loss on IR64 rice when whorl maggot (Wm) and defoliators (Def) were articially infested as individual species or combined using data from the 90 kg N/ha treatment in the damage function trials, Zaragoza, Nueva Ecija, 1989 wet and 1990 dry seasons. Damaged leaves (% at 35 d after transplanting)1 Combined infestation (WmDef) Yield loss (%)1 Combined infestation (WmDef)

Crop

Wm (A)

Def (B)

Sum (AB)

Wm (C)

Def (D)

Sum (CD)

Wet season 34.8+14.8 a 31.7+14.0 a 66.6+24.8 b 49.3+19.9 ab 4.6+5.2 a 74.5+6.8 a 0.1+7.7 a 27.0+13.6 b Dry season 24.7+11.2 a 20.7+9.5 a 45.4+20.3 b 40.9+15.7 b 11.7+4.3 a 6.1+4.9 a 17.8+9.6 ab 29.6+11.2 b
1 Data are averages of six replicates of 25 hills per 1-m2 plots at four seedlings per hill. Eight whorl maggot eggs or two 2nd to 3rd instar defoliator larvae were placed per hill on 20 hills 7 d after transplanting (DT) and again on 12 hills 10 DT per replicate in the individual pest treatments but combined in the multiple pest treatment. In a row, means+SEM, followed by a dierent letter are signicantly dierent (P  0.05) by LSD test. Each treatment consisted of 150 hills that covered a wide range of infestation levels per pest. Yield was taken on a per-hill basis. Percentage yield loss was calculated for each pest by subtracting the mean yield of damaged hills from that of the undamaged hills divided by the undamaged hills and multiplied by 100.

The dry season results of the damage function trials mirrored those of the wet season. Losses ranged from 26.3 to 29.5% deadhearts whiteheads from individual growth stages infested separately, whereas when infested together (51.6%), the damage level was similar to both summed (55.8%), thus were additive. The yield loss from the infestations considered in each growth stage separately (14.7 and 19.5%) was signicantly lower than from the combined infestation (29.6%) or when summed (34.2%), indicating losses were also additive. 3.3. Combination of leaolder in two growth stages

Leaolder larvae were also infested in either the reproductive or ripening stage or both Zaragoza damage function experiments over two seasons. In the wet season, the percentage of damaged leaves (26.8 and 28.8%) was signicantly lower than when infested in both stages (46.5% damaged leaves) which was statistically similar to both summed (55.6%) (Table 5). Yield losses from individual growth stage infestation when added (9.9 13.2 23.1%) were statistically equivalent to the loss from the combined infestation (23.6%), indicating an additive response. In the dry season, damage from individual growth stage infestation (25.8 and 26.8%) was statistically lower than from that of the combined infestation (50.6%). The sum was statistically equal to the combination (52.6%) indicating an additive eect. Yield loss was also additive, as losses from individual growth stages (10.5 and 12.4%) were half of those from the combined growth stage infestation (19.7%), but not signicantly dierent from the sum (22.9%). 3.4. Combination of defoliators, stemborer, and leaolder infestation on damage and yield A small-plot trial in Guimba was established early in the dry season to test the eect of combinations of insect pests on the resulting damage levels and yield loss. Natural infestation of each pest was at very low

levels (Table 6) and thus did not bias the trial. When defoliators were the sole pest, their combined infestation averaged 31.6% damaged leaves which, was similar to other treatments where damage ranged from 29.4 to 35.5% damaged leaves. Although substantially above the action threshold level (410% damaged leaves) (Litsinger et al. 2006a), yield loss from defoliators (71.8%) was insignicant. Leaolder infestations ranged from 14.4 to 21.2% damaged leaves in the various treatments, just above the action threshold of 415% (Litsinger et al. 2006b). As an only pest, it caused an insignicant 10.3% loss. On the other hand, stemborer deadhearts caused signicant yield loss (19.4%) during the reproductive growth stage when infestations ranged from 12.9 to 17.5% among treatments. The action threshold for this growth stage was 425% deadhearts (Litsinger et al. 2006c). Whiteheads represented stemborer damage in the ripening stage but also included counts of deadhearts that aected the younger tillers in each hill. The action threshold is lower during the ripening stage (410%) when damage levels ranged from 6.4 to 8.9%, and at 8.1% caused an insignicant loss of 15.0%. In the rst combination was defoliators leaffolder and when infested individually defoliators damaged 31.6% of leaves while leaolder damaged 16.2% summing to 47.8%. In the combined infestation we note a sum of 46.8% (32.4% from defoliators 14.4% from leaolder), which compares well with 47.8% indicating additivity. When combined there was an insignicant loss of 14.8%. Adding the individual losses equals 8.5% (71.8 10.3); losses from both pests individually and combined were not signicantly dierent. As the combination was almost twice that of each individually, it was deemed additive. The lack of signicant loss was probably due to the fact that the damage from each pest occurred at dierent growth stages. The combination of defoliators whiteheads also registered an insignicant loss of 12.1%. The total was also additive 13.2% (71.8 15). Likewise damage occurred in two dierent growth stages. The

Table 4. Comparison of the level of damage and yield loss on IR64 when stemborer was infested in the reproductive or ripening stage or the combination using data from the 90 kg N/ha treatment in the articial infestation trials, Zaragoza, Nueva Ecija 1989 wet and 1990 dry seasons. Yield loss (%)1

Deadhearts whiteheads (%)1

Crop 36.2+16.3 b 55.8+22.2 b 42.7+19.9 b 51.6+22.4 b 18.8+6.7 a 14.7+9.7 a 22.4+8.0 a 19.5+7.7 a 41.2+19.4 b 34.2+20.4 b

Reproductive (63 DT) (A) Sum (A B) Reproductive (C) Ripening (D) Sum (C D)

Ripening (10 d before harvest) (B)

Infested at both reproductive ripening

Infested at both reproductive ripening 37.2+18.6 b 29.6+18.0 b

Wet season Dry season

18.5+9.8 a 26.3+12.5 a

17.7+8.1 a 29.5+16.9 a

1 Data are averages of six replicates of 25 hills per 1-m2 replicate of four seedlings per hill. Three medium sized yellow stemborer egg masses were infested per 25 hills at panicle initiation at 35 days after transplanting (DT) and again on 12 hills 42 DT per replicate in the reproductive stage or at panicle exsertion (56 DT) and again on 12 hills (63 DT) for the ripening stage or combined in the multiple infestation treatment. In a row, means+SEM, followed by a dierent letter are signicantly dierent (P  0.05) by LSD test. Each treatment consisted of 150 hills that covered a wide range of infestation levels per pest. Yield was taken on a per-hill basis. Percentage yield loss was calculated for each pest by subtracting the mean yield of damaged hills from that of the undamaged hills divided by the undamaged hills and multiplied by 100.

Table 5. Comparison of the level of damage and yield loss on IR64 rice when leaolder larvae were articially infested on either the reproductive or ripening stages or the combination of both ages as a third treatment using data from the 90 kg N/ha treatment in damage function trials, Zaragoza, Nueva Ecija 1989 wet and 1990 dry seasons. Damaged leaves (%)1 Sum (A B) 55.6+20.3 b 52.6+23.3 b Infested at both crop ages4 46.5+18.7 b 50.6+19.9 b Reproductive (C) 9.9+7.5 a 10.5+7.9 a Yield loss (%)1 Ripening (D) 13.2+9.9 a 12.4+11.3 a Sum (C D) 23.1+9.6 b 22.9+7.7 b Infested at both crop ages4 23.6+11.2 b 19.7+15.5 b

Crop

Reproductive (63 DT) (A)2

Ripening (10 d before harvest) (B)3

Wet season Dry season

28.8+16.5 a 25.8+16.7 a

26.8+10.7 a 26.8+13.9 a

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1 Data are averages of six replicates of 25 hill (1-m2) plots sown at four seedlings per hill. Eight 2nd-3rd instar leaolder larvae were placed per hill on 20 hills 35 d after transplanting (DT) and again on 12 hills at 45 DT per replicate in the rst treatment and similarly again at 56 DT and then on 12 hills at 63DT in the second treatment. The third treatment was the combination of the two crop age infestations. In a row, means+SEM, followed by a dierent letter are signicantly dierent (P  0.05) by LSD test; 2Sampled at 56 DT; 3Sampled 10 d before harvest; 4Sum of damaged leaves from both crop ages. Each treatment consisted of 150 hills that covered a wide range of infestation levels per pest. Yield was taken on a per-hill basis. Percentage yield loss was calculated for each pest by subtracting the mean yield of damaged hills from that of the undamaged hills divided by the undamaged hills and multiplied by 100.

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J.A. Litsinger et al. The combination of four pest stresses, although produced the highest percentage loss of 40%, it was very similar to the sum of the individual losses at 42.9% (71.8% 10.3% 15.0% 19.4%) thus indicating additivity. Statistically the 40% loss was equal to both triple combinations (26.127.6%), therefore losses seemed to reach a plateau. 3.5. Stemborer damage combined with a weed, a disease, and drought stress on yield In this trial conducted at Guimba we look at the combined eects of an insect (stemborer whiteheads), sheath blight disease, Echinochloa weed, and drought stress on yield. Whitehead damage from the articial infestation ranged from 9.4 to 14.7% that included a 1.3% natural baseline infestation (Table 7). Whitehead damage was somewhat higher than in the previous trial, but in this trial, yield loss (71.2%) was insignicant. The average level of damage from sheath blight was 27% tillers infected. Of those tillers, 55% of the tiller area was diseased. But this disease incidence was considered to be moderate (Elazegui et al. 1990), and indeed the yield was statistically equal to the untreated control. Echinochloa weed averaged 11 plants/m2, which is also considered a moderate infestation (Elazegui et al. 1990). The average area covered below the canopy in younger rice was 37%, while 46% of the canopy was shaded in the older crop. Yield loss of 5.6% from Echinochloa infestation alone also was insignicant. The degree of drought stress was not meant to be severe, as that would overwhelm all other imposed stresses. Therefore water was withheld for two 1-week

combination of leaolders whiteheads occurred in the ripening stage with a resulting signicant 25.5% yield loss. But when the individual losses are summed it showed additivity 25.3% (10.3 15). The combined infestation of whiteheads deadhearts resulted in 23.9% (17.5% deadhearts 6.4% whiteheads). Adding the damage levels when infested separately we get 21.0% (12.9% deadhearts 8.1% whiteheads). Thus an additive relationship is indicated. The combination of deadhearts whiteheads resulted in one of the highest losses (37.6%), signicant over either alone, but again the total was almost equal to the individual losses summed 34.4% (19.4% 15.0%). We saw that deadheart damage alone caused signicant yield loss and thus the added pressure in the ripening stage accentuated it. The triple combination of defoliators leaolders whiteheads caused a signicant 26.1% loss. The individual losses equalled 23.5% (71.8% 10.3% 15.0%) showing additivity. The dual combination of leaolders whiteheads alone produced a signicant loss of 25.5%, but since the loss from defoliators alone was only 1.8%, adding defoliator damage did not increase loss. The triple combination of leaolders deadhearts whiteheads registered a 27.6% loss, but the sum of the losses of the three individual pests was 44.7% (10.3% 15.0% 19.4%) which would be marginally antagonistic based on the statistical analysis, as just the dual combination of deadhearts whiteheads produced a 37.6% loss. Adding leaolder damage to that of deadhearts whiteheads (27.6% loss) is not statistically dierent from that of only deadhearts whiteheads (37.6% loss), but is from deadhearts (19.4% loss) or whiteheads (15.0%) alone.

Table 6. Eect of articially infesting combinations of dierent insect pest species on yield of IR64 rice, Guimba, Nueva Ecija, Philippines, 1992 dry season. Stemborer (%) Defoliator damaged Leaolder leaves (%) damaged ag Deadhearts (5 WT) leaves (%) (9 WT) Whiteheads 3.5+1.1 c 31.6+5.7 ab 0.7+0.5 c 3.0+0.9 c 4.7+1.3 c 32.4+8.4 a 35.5+5.9 a 2.3+0.8 c 2.9+1.7 c 33.7+7.3 a 1.4+1.0 c 29.4+5.6 b 50.0001 11.12 33 0.1+0.2 b 0+0.3 b 16.2+1.4 a 0+0.1 b 0+0 b 14.4+0.2 b 0.1+0.2 b 15.7+1.3 a 0+0.1 b 21.2+2.4 a 15.4+1.9 a 17.7+3.3 a 50.0001 9.8 33 2.3+1.4 c 0.5+0.3 c 0+0.1 c 12.9+1.3 b 0.7+0.4 c 1.3+0.6 c 3.9+1.8 c 2.3+1.8 c 17.5+5.6 a 1.9+0.5 c 13.1+4.1 b 13.6+3.8 b 50.0001 8.57 33 1.9+0.7 d 1.6+0.9 d 2.9+1.7 d 2.4+0.9 d 8.1+2.2 ab 1.4+0.8 d 6.3+2.5 ab 6.9+3.0 ab 6.4+1.4 bc 5.8+2.6 bc 5.3+1.4 bc 8.9+2.6 a 0.002 7.55 33 Sum of individual insects Yield (%) Relationship loss (%) a a ab b ab ab ab bc c bc bc c 1.8 10.3 19.4 15.0 14.8 12.1 25.5 37.6 26.1 27.6 40.0

Treatments Natural infestation Defoliator (Def) Leaolder (LF) Deadhearts (DH) Whiteheads (WH) Def LF Def WH LF WH DH WH Def LF WH LF DH WH Def LF DH WH P F df
1

Yield (t/ha) 4.13+0.31 4.20+0.34 3.70+0.29 3.33+0.43 3.51+0.41 3.52+0.37 3.63+0.26 3.08+0.25 2.58+0.42 3.05+0.19 2.99+0.24 2.48+0.17 0.001 9.32 33

13.2 25.3 34.4 23.5 44.7 42.9

Additive Additive Additive Additive Antagonistic Additive

Plot size was 50 m2 but the center 25m2 was infested with insects under a wooden frame nylon mesh cage removed after one week. Defoliators were a mixture of 3rd and 4th instar Naranga and Rivula larvae infested at 4 per hill at 3 weeks after transplanting (WT). Leaolder was similarly infested as 4 late instar larvae per hill at 5 WT. Stemborer was infested as 3 medium egg masses per 1-m2 at 3 (deadhearts) or 6 (whiteheads) WT; 2 The randomised complete block experiment of 12 treatments was replicated three times. In columns, means+SEM, followed by a dierent letter are signicantly dierent (P  0.05) by LSD test.

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Table 7. The eect of articially infesting stemborer alone or combined with drought stress, a weed, or a plant disease on yield in eld plots of IR64 rice, Guimba, Nueva Ecija, Philippines, 1992 dry season1. Stemborer whiteheads (%) 1.3+0.5 9.4+2.3 0.6+0.5 0.7+0.9 5.4+1.4 13.9+4.6 12.3+3.8 14.7+4.4 12.2+5.1 0.03 6.99 24 c ab c c b a a a a Sum of individual stresses (%)

Treatment2 Natural infestation Stemborer whiteheads (WH) Sheath blight (ShB) Echinochloa (Ech) Drought stress (DS) Ech WH ShB WH DS WH Ech ShB DS WH P F df

Yield (t/ha) 5.14+0.38 a 5.20+0.44 a 5.07+0.35 a 4.85+24 ab 4.57+0.32 b 4.60+0.21 b 4.58+0.33 b 4.03+0.18 c 3.67+0.20 d 50.0001 8.53 24

Yield loss (%) 71.2 1.4 5.6 11.1 10.5 10.9 21.6 28.6

Relationship

4.4 0.2 9.9 16.9

Synergistic Synergistic Synergistic Synergistic

1 Average of four replications in a randomised complete block design. In a column, means+SEM in a column followed by a dierent letter are signicantly dierent (P  0.05) by LSD test.Plot size was 16 m2; 23 Stemborer egg masses/m2 at 6 weeks after transplanting (WT), 200 mg of sheath blight sclerotia inoculated per hill at 6 WT, 10 weeds/m2 transplanted at 2 WT, irrigation water withheld for two weeks each in the reproductive and ripening stages.

periods. The cracking allowed more drying conditions to reach further down the soil prole. In irrigated rice, roots are shallow, mostly occurring above the natural plow pan. Still drought stress alone created a signicant 11.1% loss. Whiteheads combined with Echinochloa caused a signicant loss of 10.5%. This compares with 4.4% from the sum of each (71.2% 5.6%) indicating a synergistic response from the combination. Whiteheads combined with sheath blight also caused a signicant loss of 10.9%. When we add the loss of each individually (71.2% 1.4%) the sum is 0.2%, which also indicated synergism. Whiteheads combined with drought stress caused a much greater loss of 21.6%. When we add the losses from individual treatments (71.2% 11.1%), the sum equals 9.9% again indicating a synergistic crop response. The highest loss came from the combination of the four stresses (28.6%), which was signicantly more than any other combination. When we add the component losses (71.2% 1.4 5.6% 11.1%) we get 16.9% once more showing synergism. 4. Discussion 4.1. Multiple insect pest infestations 4.1.1. Whorl maggot and defoliators Four trials/treatments compared whorl maggot and defoliator damage from individual species and joint infestations (Tables 1 and 3). Three trials showed that joint damage was additive with only the wet season trial in Zaragoza being statistically intermediate between additive and antagonistic. Antagonism could be explained as passive competition from inadvertent consumption of whorl maggot eggs (laid openly on leaf surfaces) during defoliator larval feeding. Another reason may be due to the earlier colonisation of whorl

maggot. As whorl maggot larval feeding is internal, it is unlikely to directly interact with defoliators. However, yield loss results from the four trials/ treatments showed positive synergism when both whorl maggot and defoliators were combined. It had been postulated that such a relationship was occurring in earlier on-farm, yield-loss studies (Litsinger et al. 2006a). Before elaborating an hypothesis to explain this phenomenon, we need to reconcile our ndings with the whorl maggot literature in the Philippines, most of which concludes that whorl maggot does not cause yield loss even under heavy infestation. Ferino (1968), who rst studied the whorl maggot, recorded losses 440% at the University of the Philippines Experimental Station next to IRRI in Los Banos in Laguna province. Litsinger et al. (1987) also documented signicant losses that averaged up to 15% in some sites in on-farm studies. On the other hand, Valencia and Mochida (1985), Viajante and Heinrichs (1986), and Shepard et al. (1990), all of whom performed yield loss trials on the IRRI Farm, found that even crops suering 460% damaged leaves did not result in signicant loss. To explain this contradiction, we rst note dierences in the rice growing conditions between the IRRI Farm and the other experimental sites. On the IRRI Farm and in Ferinos trials in Los Banos, the only vegetative pest of signicance was whorl maggot as infestations of defoliators were rare. High populations of stemborers occurred in the vegetative stage along with whorl maggot in the 1960s in Los Banos when Ferino undertook his research. In on-farm trials outside of Los Banos, whorl maggot invariably occurred in association with defoliators that normally comprised 2025% damaged leaves from whorl maggot plus 10% damaged leaves from defoliators in sites with highest densities (Litsinger et al. 2006a). Ferinos

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J.A. Litsinger et al. single stage infestations. In the three trials shown in Tables 4 and 6 the answer was no, as all the results were additive. The only surprising result was that, for a given infestation level, losses were not greater in the ripening stage, known from other studies to be less able to compensate (Bandong and Litsinger 2005). The ability to compensate may have been compromised due to the agronomic practices in our trials where, 30-day-old seedlings pulled from hard clay seedbeds were transplanted thus transplanting shock was severe. In addition, IR64 is an early maturing variety (117 days) that limits compensation compared to longer maturing varieties (Litsinger 1993). It is also likely that root-feeding nematodes were present (Prot et al. 1994). Each of these factors would increase the number of stresses that could have further reduced compensation. 4.1.3. Leaolder

losses were measured from insecticide trials that employed BPI76 variety, highly susceptible to stemborers. During those years, losses to stemborers on the IRRI Farm were very high (normally 430% based on insecticide trials), probably due to the susceptible varieties grown at the time (Litsinger 2008). In addition in an articially infested IRRI Farm trial (IRRI 1983), the combination of whorl maggot and yellow stemborer produced the greatest synergistic loss (59%) compared to 27% when added individually. Thus it is likely that the combination of whorl maggot and stemborers caused synergistic loss in Ferinos trials. Litsinger (2009) hypothesised that transplanting shock, combined with whorl maggot and defoliator injury, could explain the higher yield losses observed outside of the IRRI Farm. Transplanting shock refers to the root injury that results when seedlings are pulled from the nursery bed plus the rough handling they receive before being transplanted (Matsushima 1980). In addition, roots are turned upside down in the mud during transplanting as seedlings are held at the base of the tillers because this method is quicker. Defoliation injury also reduces root growth, further extending the recovery period which can take 2 weeks or more. This is important because during the recovery period, seedlings lose their ability to compensate from insect injury. As Filipino farmers do not thoroughly prepare their seedling nursery bed nor apply organic matter, roots become cemented into the heavy clay. Therefore, farmers are forced to transplant 30-day-old seedlings that are large enough to tolerate the force needed to uproot the plants without being torn in half, resulting in severe root injury. However, optimal tillering occurs from transplanting 20-day-old seedlings, with tillering rate being proportionally reduced for each additional days delay (DeDatta 1981). On the IRRI Farm, there is a communal seedbed where the soil is more thoroughly prepared, achieving a slurry-like consistency, thus pulling young seedlings causes minimal root injury. Therefore, the following hypotheses are oered to reconcile the contradiction in yield loss results. On the IRRI Farm, rice crops since the 1960s compensate more fully because: (1) whorl maggot occurs as a single pest, (2) transplanting shock is minimal, and (3) young seedlings tiller more. In Central Luzon, synergistic loss occurs from: (1) the combination of whorl maggot with defoliators which reduces photosynthesis and root growth due to prolonged transplanting shock and (2) the use of older seedlings which limits tillering. 4.1.2. Stemborer

Colonisation of leaolder occurs throughout the rice crop, but infestations are generally greater in the reproductive and ripening stages (Litsinger et al. 2006b). From trials in the wet and dry seasons in Zaragoza, leaolder infestation at each of the reproductive and ripening stages showed additivity in terms of damage or yield loss when infestation was combined (Table 5). Just as with stemborer, the result seems surprising in light of the reported greater susceptibility of the ripening stage crop (Heong 1990). As with stemborers, agronomic practices followed in the trials may have impinged the crops ability to compensate. 4.2. Insect pest infestations combined with weeds and disease 4.2.1. Weeds Weeds compete with rice for water, nutrients, solar radiation, and space that collectively compromise numerous plant physiological processes of the rice plant (DeDatta 1981). If uncontrolled, weeds can lead to severe losses, thus this guild is a perennial major constraint to yield, more so than insect pests or diseases. Higgins et al. (1983) found that compensatory plant re-growth from defoliation injury may be exacerbated if the plant is also under stress from weeds. Savary et al. (1994) noted lowest yields were associated with stress from weed species such as Echinochloa that reach above the canopy. Echinochloa, which is given the local name antenna by farmers, is dicult for hand-weeders to distinguish from rice and thus often goes uncontrolled. In the multi-pest infestation trial in Guimba, transplanted Echinochloa was at such a level that no signicant loss occurred as a sole pest. Signicant loss only was registered when the weed occurred with whitehead injury (Table 7). In Central Luzon, the only insect pest Savary et al. (1994) found

Rice stemborers in the Philippines predominantly attack the reproductive and ripening stages (Litsinger et al. 2006c). The question being asked is that, in a multiple rice growth stage infestation, will infesting two stages lead to greater damage than the sum of the

International Journal of Pest Management associated with low yields was the combination of stemborer and weeds. 4.2.2. Sheath blight disease

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benets as a nematode suppressant in irrigated rice elds (Prot et al. 1992). 4.3.2. Solar radiation

Rice fungal diseases in the Philippines are generally less of a problem than in other Asian countries due to the fact that the popular IR-varieties were bred in the Philippines and therefore selection occurred for lines with resistance or tolerance to local strains (Khush 1989). There are half a dozen rice diseases that occur particularly in the wet season due to monsoon rainfall and strong winds (Ou 1972). Such storms aid dispersal of pathogens via water and air as high winds cause leaves to rub together creating entry wounds. Savary et al. (1994) found that surprisingly sheath blight was associated with highest yields in correspondence analysis studies in Nueva Ecija. It is likely that the high yields were due to high N application that also may have promoted the disease (Ou 1972). In the current study (Table 7), sheath blight alone caused only 1.4% yield loss, but when combined with whiteheads caused a synergistic loss of 10.9%. In combination with three other stresses, the loss was even greater. In another study, Willocquet et al. (2002) found highest losses in the combination of stemborers and sheath blight. 4.3. Insect pest infestations combined with abiotic factors Nitrogen, solar radiation, and water are the key inputs of photosynthesis and rice growth, thus, when any of these factors is decient in the presence of insect pest damage, the combination should lead to high losses. 4.3.1. Nitrogen

Solar radiation is one of the most important abiotic factors aecting rice yield (Yoshida 1981). In the Philippines, dry season yields are typically 20% higher than those of the wet season mainly due to greater solar radiation (Litsinger et al. 2005). In our studies in Zaragoza, the average tiller density per hill at maximum tillering in the 90 kg N/ha weed-free treatments was 44% higher in the dry season (31.3 tillers/hill) than the wet season (21.8) (P 5 0.0001, F 200.5, n 324). The comparison of number of leaves per hill was 124.5 vs. 100.2 (P 5 0.0001, F 51.45, n 324), a dierence of 24%. Better growth in the dry season was due to a fuller rice canopy to capture incident radiation, resulting in greater panicle densities and a higher percentage of lled grains (DeDatta 1981). An actinograph set out in the agro-met station in nearby Guimba in 19891990 recorded an average of 28% more solar radiation in the dry season. Low solar radiation is due to a combination of cloudy weather and short day-lengths as the wet season crop is typically in the ripening stage from September to November. 4.3.3. Drought

Applied N increases tiller, leaf, and spikelet densities that lead to increased yield (DeDatta 1981). Boling et al. (2004) demonstrated that increasingly N rates promoted compensation from insect pest damage. Two trials in the current study tested the benet of applied N in bolstering the crops ability to compensate from a range of stresses. In the rst trial (Table 2), crops with an organic N source, consistently out-yielded crops with inorganic N when infested with whorl maggot, defoliators, or both combined. Inorganic N, as a paddy water broadcast, lasts less than a week in rice elds (DeDatta 1981). Ishikura (1967) summarised research that noted organic N increased the compensatory ability of rice plants to striped stemborer (Chilo suppressalis [Walker]) injury. Organic N, by being released more slowly and continuously than an inorganic source, was seen as improving N usage eciency as well as reducing the optimal dosage for inorganic N (DeDatta 1981). Sesbania oers additional

Drought stress can develop in irrigated rice areas from deterioration of the canal infrastructure, lack of rainfall in the watershed, or power shortage in areas serviced by electric pumps. Working in Java, Boling et al. (2004) found insect pest and disease losses were exacerbated by drought stress. In an earlier study in the Philippines, stemborer injury combined with drought caused highest yield losses in a long-term, multilocation study (Litsinger et al. 2005). In the Guimba trial (Table 7), drought was the only stress that caused signicant yield loss as a single factor, and when associated with stemborer injury, drought led to the greatest loss of any two combined stresses. In this study, drought was articially created to occur at two brief periods in the late growth stages. Yoshida (1981) noted rice is most susceptible to drought if it occurs during grain lling which was one of the stages included in the Guimba study. Due to the fact that most physiological processes require water, it is not surprising that there is low capacity of rice plants to overcome its deciency; even more so given that drought is one of the major stresses for which rice has the lowest tolerance within the major world cereals (Yoshida 1981). 4.4. Multiple infestations Walker (1975) was one of the rst to point out the problem in assessing crop loss from a particular insect

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J.A. Litsinger et al. reproductive stage did not predispose the ripening stage to greater injury. This contradicted a report from Schoeneweiss (1975) who found repeated bouts of defoliation over the life of dierent plant species resulted in synergistic loss. Antagonism can mean that: (1) one stress is competing with another for a common plant resource or (2) the capacity for compensation from one stress is compromised by another stress. The rst method is straightforward and the example of defoliatiors consuming whorl maggot eggs was already given. The following two examples involve interference with the process of compensation which may be less commonly appreciated. Johnson et al. (1986) showed that yield increase from fungicide control of potato early blight Alternaria solani (Ell. & Mart.) Jones & Grout only was realised if soils were rst fumigated against Verticillium dahliae Kleb wilt at the seedling stage. The reason was that seedling mortality from wilt reduced plant density to a level that the crop could not compensate adequately from the improved blight protection in later stages. A further example is from dryland rice where a mixture of biotic and abiotic stresses occurred in an area as a result of highly eroded acidic soils (Litsinger et al. 2009). Applying an insecticide seed treatment against rice seedling maggot Atherigona oryzae Malloch gave a 3.5-fold increase in yield, but a 7-fold increase occurred if wood ash and urea fertiliser were applied without insecticide. Thus with adequate plant nutrition, the injury from seedling maggot could be compensated by the high tillering variety. In the Guimba trial, there were two types of injuries caused by defoliators, leaolders, and stemborers in the triple combination. Defoliators and leaolders remove photosynthetic capacity, whereas stemborers sever vascular tissue leading to wilt and eventual tiller loss. We hypothesised potential synergistic loss arises if two pests, each causing a dierent mode of injury, attacked the same growth stage (Litsinger 1991). This result occurred with whorl maggot defoliators, but not with leaolders stemborers. The latter combination occurred three times in the Guimba trial, where twice the eect was additive, while in the third it was marginally antagonistic. As was stated earlier, the lack of consistency in response may be due to dierences in pest density or from dierences in the occurrence of stresses outside of the experimental design. In the Guimba study we combined whiteheads with other stresses (drought, weeds, or sheath blight) as well as all four together (Table 7). The synergistic results we report are in variance with other previously cited studies of multiple infestations on rice. We postulate that synergistic loss came about as a result of dierent physiological processes being involved from each stress. Drought removes water from the plant that aects every physiological process. Weeds also negatively aect plant processes in nutrient and water

pest due to the presence of other pests that typically occur in the eld that could bias loss estimation. Loss from insect pests does not occur in isolation but in association with not only other kinds of pests, but from a multitude of abiotic factors such as nutrients, drought, solar radiation, etc. where the contribution of each may or may not be additive. We documented a variety of yield loss interactions that ranged from additive, antagonistic, or synergistic in the eld from a wide array of stresses. Johnson (1987), in a literature search of multiple pest interactions that included plant diseases, weeds, and insects, noted 57% of relationships on a variety of crops were antagonistic with the balance being evenly divided among additive and synergistic. Pinnschmidt et al. (1995) and Willocquet et al. (2000), using computer simulations, concluded that losses from multiple pest infestations from weeds, sheath blight, and stemborers usually exhibited antagonistic responses, even when the same combinations were tested at twice the infestation levels. Our eld trial in Guimba, on the other hand, showed synergistic relationships from the same group of pests, possibly indicating that the crops were under greater stress from other causes as well as those manipulated in the trials. We have already given a list of possible causes, which no doubt is incomplete. In our trials, results pointed out that for most combinations of insect pests, irrespective of the number of species involved, losses were additive. There were only two exceptions: (1) whorl maggot defoliators as synergistic and (2) the triple combination of leaolder deadhearts whiteheads that were marginally antagonistic. The triple combination was most interesting because another such combination of defoliators deadhearts whiteheads and the quadruple combination were additive. Notably, pest abundance was lower in the antagonistic triple combination compared to those in the other combinations (Table 6). Additionally yield loss was notably higher from the dual combination of deadhearts whiteheads than the antagonistic triple combination that included both forms of stemborer damage plus leaolder. This may mean that there might have been an additive outcome if pest densities were greater. The fact that Willocquet et al. (2000) found doubling pest densities did not change the yield loss relationship, points to the need to identify the plant physiological pathways aected by pest combinations and understand how these aect loss. How is it that sheath blight in one experiment is associated with highest yields while in the next is responsible for synergistic losses? This question is made all the more dicult as each pest may aect more than one plant physiological pathway. Stemborers or leaolders, each sequentially attacking two crop stages, caused yield loss no dierent than the sum of each stage attacked individually. Thus the combined damage was additive for each pest. This result implied that a crop weakened by damage in the

International Journal of Pest Management supply as well as reducing solar radiation. Other explanations are possible. Despite the association of sheath blight with high yields by Savary et al. (1994), Pinnschmidt et al. (1995) noted that the type of injury caused by the pathogen was complex, more than just removal of photosynthetic area. This further underscores the need to better understand the eect of each stress on the plants physiology. 4.5. Implications for pest management

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Our trials have demonstrated that the extent of yield loss depends signicantly on the pest composition, and intensity of injury and the plant physiological process aected, as well as the rice production environment. Evidence indicates that the more stresses present and the greater their intensity, the greater would be the loss. Rice damage functions show that increase pest densities reduce the compensatory ability of the crop (Litsinger et al. 2011), and we have shown that synergistic losses are more likely when insect pest injury is linked with injury from other pests or abiotic factors. On the other hand, certain crop management practices can bolster the crops compensatory capacity. Litsinger (1993) provided evidence that selecting medium maturing varieties, using adequate N levels, and sowing at higher densities enhanced the crops ability to tolerate pest injury. Both papers in this study illustrate the tension that exists between these diametrically opposing forces that act on the crop with the resulting yield being determined by the balance from pull from conditions that stress the crop against the counter-pull of compensatory factors. That there is such a yield equation is not a new insight, but the intensity of some of the common stresses, when combined, we believe is. Also a new concept is that once synergistic stresses are relieved, under certain conditions, a synergistic yield gain can be realised (Litsinger 2009). Before this study, whorl maggot was debunked as an economic pest, and in other studies on multiple infestations of common stresses, losses were shown to be mostly additive or antagonistic (Pinnschmidt et al. 1995; Savary et al. 1997). We noted that many common insect pests, even when at sub-economic densities individually, resulted in additive or synergistic losses when combined. Highest losses consistently came from insect pests combined with weeds, disease, or drought. Our conclusions are supported by the synergistic losses reported in IRRI (1983, 1984). We now believe such synergistic interaction accounts for much of the yield variability we noted in rice farming communities as well as the unexplained high yield losses mentioned in Litsinger (2009). These losses were unexplained because a large yield gain occurred in the insecticide-protected plot over the untreated from 3 to 4 insect pests, all at densities that were below action threshold levels, just as in the above IRRI studies.

Most of the unexpected losses were from modern rices, but one study (Litsinger et al. 2009) showed the phenomenon also occurred with traditional tall varieties. Tall, low-tillering rices compensate by lling more grains and producing larger grains and, being longer maturing, they provide more time to compensate. Modern rices are earlier maturing, but can also ll more grains per area and tiller more. Modern rices, known to be particularly responsive to improved crop management (DeDatta 1981), are equally negatively or positively responsive to stresses, particularly when they are multiple. Multiple stress of insect pest damage in conjunction with other pest groups or abiotic causes is likely to lead to synergistic gain when insect injury is relieved. Synergistic yield gain not only can be due to relief from stresses caused by insects but also from other sources. This phenomenon may also explain the unexpected high yield response of the farmers practice reported in Litsinger et al. (2005). In the latter case, farmers practice is 34 low dosage insecticide sprays using broad-spectrum materials, which often showed signicant yield increases in the presence of low pest mortality rates. The unexpected high yield increase we believe would only occur when a requisite number of compensatory forces are present. We believe varieties bred with a Bt gene would particularly promote this synergistic yield gain due to control of lepidopterous insect pests such as defoliators, stemborers and leaolders that would allow greater compensatory benet to overcome other non-insect pest stresses. We have outlined a mechanism to explain the wide range in yield experienced in a typical rice growing community in the Philippines. A basis for this hypothesis is that crop stresses do not occur uniformly in a farm community. In the wet season, stress occurs from ooding, typhoon wind damage, and reduced solar radiation, especially during the ripening stage when typhoons are more frequent. There is always variation among farmers in planting date, sometimes quite extensive. Evans and DeDatta (1979) noted that dierences in rice yields could be 30% due to variation in solar radiation just from planting a month later or earlier. Zinc deciency can occur in low-lying elds (DeDatta 1981). We noted how important weed control is, especially in the dry season. Weeds proliferate if the farmer is unable to organise hired labourers in a timely fashion. Farmers can run arrears in paying an electrical bill for the irrigation pump, or water stress can occur from a number of other causes. We noted drought, in combination with insect injury, is often associated with especially low yields. Fertiliser may not have been available on time, or it may have been adulterated, or the farmer could not get credit. There are many possible stresses that are beyond the control of farmers to manage, even a well-educated farmer. If the farmer sows early maturing varieties or uses less fertiliser, many of the stresses mentioned can

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J.A. Litsinger et al. We conclude that at least for stemborers, combinations of stresses can produce losses that can be antagonistic, additive or synergistic, thus this relationship appears to be highly dynamic and conditioned with each situation. Our results show that for a given density, the loss from a given pest can change in its association with each set of stresses as well as with each set of compensatory factors that are present. We not only have to determine the potential losses as a result of these dierent sets of stresses and compensatory factors, but what the outcome would be from dierent intensities of each component in the mix. Thus empirical approaches such as those employed in this study can only demonstrate trends, as the number of treatments from the potential permutations of factors dees experimental eld plot methods to solve (Poston et al. 1983). Clearly the arguments of the crop modellers have merit, and who approach the problem from the more fundamental perspective of plant physiology.

be augmented. In the following season, however, the farmers fortunes can quickly reverse (Litsinger 2009). For the many reasons we have shown, yield can dier eld-to-eld and even in the same eld each season. Even the same farmer can be in the upper onethird of the yield frequency curve (Pingali et al. 1990) one season, and be in the bottom one-third the next. This result has consequences for farmer training strategies as all farmers need to be trained. Our research supports Savary et al. (2006) who concluded that undertaking a management strategy based on rice injury and crop environment proles is more relevant than that of individual pest injuries. Knowledge of such broad-based causes of crop loss, therefore provides entry points for management. In order to implement such a new strategy, it is imperative that the farmer rst needs to adopt as many of the preventative crop management practices as he can that have been shown to promote compensation. The more measures that he can put into practice, the higher he can raise his action threshold decision level that would trigger a corrective insecticide application. To implement the aforementioned recommendations, extension workers and farmers need to be trained to recognise the major stresses aecting the crop and to assess the importance of each in terms of potential yield loss. A farmer having good knowledge of the interactions of the various stresses that can act on his crop can only eliminate the stress that he can readily manage such as weeds, N rate, crop duration, and agronomic practices in general. In managing them, the farmer that has undertaken sound preventive practices should note that to obtain high yields he need not remove all of the stresses (Litsinger 2009). As a strategy, the farmer only needs to correct some of the stresses, and it has been proposed that the farmer should focus on the most economically manageable ones and let the crop compensate for the rest. Therefore knowing the impact of dierent combinations of stresses should therefore lead to better management decisions. Previous trials have shown that whorl maggot is dicult to control with insecticides (Litsinger et al. 2006a), as are stemborers (Litsinger et al. 2006c). As a result of this study, we note how important the whorl maggot defoliator combination can be. The farmer can ameliorate loss in this instance by lessening the impact of transplanting shock through preparing a lighter textured soil in the seedbed by using compost or, failing that, direct insecticides to the more easily controlled defoliators. Regarding stemborers, the farmer should undertake preventative measures to increase the crops ability to compensate (Litsinger 1993) rather than attempt to control them with insecticide. In addition more research should be done on the eect of seedbed production practices on the ability of the rice crop to withstand stresses after transplanting.

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