16 Plant Protection Quarterly Vo1.1 3(1) 1998 Sampling method Samples were obtained using a Ryobi Sweeper Vac (model RSVllOOA MKll) vacuum sampler modified according to Research reports Wright and Steward (1992). An empty sampling bag was placed in the vacuum sampler before each sample was taken. Ten samples at each site were taken at monthly intervals from September 1993 to The effect of non-crop vegetation on the insect pests October 1994 by applying the va cuum sampler to 30 flushing shoots from each of and their natural enemies in cashew (Anacardium five cashew trees at the middle level of the L.) tree canopy. At each sampling occasion, a occidentale plantations total of fifty evenly distributed trees were sampled at each site. The samples were R.K. Peng, K. Christian and K. Gibb, Faculty of Science, Northern Territory then frozen. After 24 hours, a ll the arthro­ University, Darwin, Northern Te rritory 0909, Australia. pods in each bag were transferred into a bottle containing 70% ethanol fo r later ex­ amination.

Abstract could provide a reservoir of natural en­ Trophic studies In order to introduce an integrated pest emies that may regulate insect pests in A flexible netting bag (45 x 28 x 18 cm) management program in cashews, the ef­ cashew plantations. The most important was used to confine insects to an a rea on fect of non-crop vegetation on the arthro­ predators of the main cashew insect pests flushing shoots of a field cashew tree to pod fauna in cashew plantations in tropi­ are green ants, Oecophylla smaragdilla determine the food habits of a variety of cal northern Australia was studied by (Fabricius) (Peng el al. 1995). The specific arthropod species under realistic condi­ taking regular vacuum samples. Where aims of this stud y were: tions. With this technique we could check cashews had rich understorey and were i. to assess whether proximity to non-crop the bag easily and transfer it to fresh flu sh­ closely surrounded by non-crop vegeta­ vegetation can increase the diversity of ing shoots when the condition of the flush­ tion, the diversity of arthropods, the ra­ arthropods, ing shoots inside the bag became poor tio of the total natural enemy numbers to ii. to determine whether non-crop vegeta­ due to insect feeding. This system was insect pests and the average yield were tion can enhance natural enemy popu­ used in four cashew phenological periods; significantly higher than where cashew lations in cashew plantations, espe­ pre-flowering (March-April), fl owering trees had no understorey and were iso­ cially the green ant population and (May- June), flowering and fruiting Oune­ lated from non-crop vegetation. We sug­ iii.todetermine whether there is a relation­ August) and ordinary flush (September­ gest that the close proximity of non-crop ship between the proximity of non-crop October) from September 1993 to August vegetation enriches the diversity of vegetation and crop yield. 1995. To determine the relationship be­ arthopods in cashew plantations by pro­ tween insect pests and their predatory ar­ viding a reservoir of natural enemies that Materials and methods thropods, each predatory species together naturally regulate insect pests and re­ with each species of insect pest was intro­ sults in an increased crop yield. Study sites duced into the bag which covered two ar­ Two study sites were used for this study: thropod free flushing shoots. These bags Introduction a two hectare section of eight-year-old were checked once a day for two days. Pi.lot cashew plantations in the Northern cashew trees a t the Wildman River Planta­ Eight fie ld observations were made to ob­ Territory of Australia have been subject to ti on (12 0 64·S, 131 0 8TE) and a two hectare serve the feeding behaviour of the main serious insect pest problems since 1988 stand of six-year-old cashew trees at the insect pests and their natural enemies dur­ (Houston and Malipatil 1991, Peng el al. Howard Springs Farm (12 0 49·S, 131 0 ing the insect pest outbreak of 1994 and 1995, Stonedahl el al. 1995). Consequently, 04'E). The Wildman River site is 90 km 1995. Observations were made during insecticides have to be regularly used to east of Howard Springs. The planting pat­ three periods (early morning, noon and ! control insect pests such as He/opeitis terns of cashew trees at both sites were early evening) and each period lasted pernicia/i, (Stonedahl. Malipatil and Hou­ similar, and both sites experienced the 1-1.5 hours. ston), Amblype/ta IIIleseell s (Distant) and same tropical wet-dry climate. The study Pellicillaria jocosatrix (Guenee). Insecticides site at Wildman River was in the centre of Arthropod identification can lead to a reduction in insect pest para­ 16 hectare of cashews (370 m away from Known cashew insect pests and their site and predator populations as well as non-crop vegetation) and had not received natural enemies were identified to species. in sect pollinator populations. It is there­ pesticides since June 1993. The study site Other arthropods were identified to spe­ fore very important to explore alternative at Howard Springs had not received pesti­ cies, genera, sub-family or family level. control methods. cides since April'1993 and was closely sur­ Cashew plantations in the Northern rounded by non-crop vegetation. At the Yield assessment Territory of Australia are surrounded by Wildman River site, ground vegetation To harvest cashews, growers wait for the non-crop vegetation such as Acacia, Euca­ under cashew trees was sparse, contain­ nuts to drop on the ground before they are lyptus, Erythrophleums, Planc110nia and ing only a small amount of grass picked up by a vacuum harvester. Eight Buchanania. The 'natural enemy hypoth­ Pellll i,etu", polys/aeilioll (L.) Schultes be­ trees at each site were randomly chosen esis' predicts that there will be a greater tween weeding periods. At the Howard for yield assessment. At the beginning of abundance and diversity of natural en­ Springs site, the ground vegetation was the fruit setting period, fallen leaves, tvvigs emies of pest insects in polycultures com­ dense and rich, dominated by P. and grass under each tree were cleared to pared to monocultures (Root 1973). We polystaeilioll, Sida spp., ealopogonill'" facilitate a late harvest. All the nuts under wished to determine whether the presence ","eunoide, (Desv.), Passifiora foelida (L.) each tree were coUected by the vacuum of non-crop vegetation near cashew trees and Hyplis sauveolells (L.) Poit. harvester and weighed separately. Plant Protection Quarterly VoI.13(1) 1998 17 Climatic data Table 1. Similarity measurement of the richness of non-crop trees close to The microclimatic data at the Wildman cashew plantations, the main insect pests and their natural enemies in River Plantation were taken from the cashew plantations between Wildman River Plantation (WRP) and Howard records of a meteorologica l stati on inside Springs (HS). the cashew plantation. The microc1imatic data at the Howard Springs site were from Type Number of species Number of species in C j the records of the meteorological station of WRP HS common between two sites Howard Springs Nature Park, 5 km from Non-crop trees 24 27 22 0.76 the study site. Insect pests 11 11 11 1.00 0.88 Statistical analysis Natural enemies 21 24 21 All the arthropods ca ught by the vacuum sampler were included in the statistical Table 2. Comparisons of the mean temperature, the mean relative humidity comparisons. The log-series index (0.) and the rainfall between Wildman River Plantation (WRP) and Howard (Fisher e/ a/. 1943) was used for the analy­ Springs (HS) from October 1993 to October 1994 using paired sample t tests. sis of diversity: S ~ 0: In(1 + N/o:), where S = number of taxa and N = number of indi­ Type Site Mean ± SEM Difference between P viduals. The greater the value of 0.., the means ± SDD more diverse is the community. The Ave. temperature (OC) WRP 26.7 ± 0.8 -0.277 ± 0.559 -1.788 0.101 Jaccard equation, C) = j/(a+b-j), was used HS 27.0 ± 0.7 to measure similarity between non-crop Ave. relative humidity (%) WRP 66.8 ± 2.9 -1.000 ± 2.582 -1.396 0.188 trees, insect pests and their natural en­ HS 67.8 ± 2.9 j = emies between the two sites, where the Rainfall (mm) WRP 94.8 ± 31.8 ·0.705 ± 1.273 -1.662 0.135 number of species in common at both HS 146.2 ± 57.9 sites, a or b = the number of species which occurred at each site (Southwood 1978). The value of C ranges from 0- 1, and the J 50 bigger the value, the more similar the two sites. The ratio data of natural enemies to pests were transformed to arcsine square root. and the rainfall data were trans­ fo rmed to natural logarithm before statis­ 40 tica l tests were applied. Paired sample t tests were used to compare the arthropod diversity, the ratio of natural enemies to insect pests and the microclimatic factors '3',..., between the two study sites. A group sam­ ..~ 30 I- ple t test was used to compare the yields ~ of the two sites. .5 .t> Results .; .. 20 I- .~ Similarity of biological and physical Q factors between two sites The numbers of non-crop tree species present between the two sites were statis­ 10 tically equivalent (C j ~ 0.76, Table 1), and the fauna of the main in sect pests and natural enemies in cashew plantations

was also equivalent (CJ = 1 and 0.88 re­ spectively, Table 1). Although the mean o temperature, the relative humidity and 9 10 12 2 3 4 5 6 7 8 9 10 the rainfall were higher at the Howard Springs site than at the Wildman River Plantation, there were no statistically sig­ Year (1993 - 1994) nificant differences between the two sites (Table 2). Figure 1. Div.ersity (log-series index with standard deviation bars) of arthropods on cashew trees between Wildman River Plantation (_) and Arthropod diversity between two sites Howard Springs (ISSSJ ) for each month. A total of 12 800 arthropods was caught, belonging to 348 taxa. These included 206 named species or genera, 131 recognisable for each month (Figure 1). For each month, In sect pests and their natural enemies at taxonomic units under sub-families or the diversity of arthropods at Howard the two sites families, three at the sub-family level and Springs was significantly greater Table 3 lists the number of individuals of eight at the family level. There were 11 (P ~ 0.002) than at Wildman River except each of the main insect pest species and main species of insect pest and 24 species for October 1994, in which the diversity at their natural enemies caught at the two of natural enemy (Table 3). Wildman River was higher than at sites. The same 11 species of insect pest Th e diversity of arthropods between Howard Springs (Figure 1). occurred at both sites, but the numbers of the two sites over one year was compared individuals were higher at Wildman River 18 Plant Protection Quarterly VoI.J3(1) 1998 than at Howard Springs, except for aphids Table 3. Abundance of main insect pests (IP) and their natural enemies and Aatids which were more numerous at (NE) collected from cashew trees by a vacuum sampler at Wildman River Howard Springs. A greater number of Plantation (WRP) and at Howard Springs (HS) from September 1993 to species of natural enemies was caught at December 1994. Howard Springs (total = 24) than at Wildman River (total = 21), and 13 of the Species Status Total number Feeding habit determined by flexible 21 natural enemy species common to both trapped at net bags and field observations sites were more abundant at Howard WRP HS Springs than at Wildman River (Table 3). The numbers of individuals of all insect Araneae pest species and their natural enemy spe­ Oxyopidae cies caught at both sites are shown for Oxyopes sp. NE 29 177 Feed on Helope/tis nymph each month in Table 4. The ratio of natural Coleoptera enemies to insect pests was significantly Coccinellidae higher at Howard Springs than at Coelophora sp. NE 2 224 Feed on aphids Wildman River (P = 0.0001). C. inaeqrmlis NE 1 12 Feed on aphids Table 5 shows the abundance of O. Cryptolaem us I1wuntrou zieri NE 49 222 Feed on mealybugs smaragdina. In each month, O. smaragdiua Rhyzobills sp. NE o 14 Feed on scales were much more abundant at Howard Scymnus sp. NE 58 77 Feed on aphids Springs than at Wildman River. It took over 15 months after the final pesticide applica­ Diptera tion at the Wildman River site before O. Syrphidae smnragdilla became common (Table 5). Eristalis sp. NE o 16 Feed on aphids Hemiptera Yield be/ween two sites Coreidae Comparison of the yield for 1993 and 1994 Amhlype/ta Illtescells IP 41 Feed on foliar and floral flushes showed that the average yield per tree at Miridae Howard Springs was significantly higher Heiopeitis perniciaiis IP 215 11 Feed on cashew shoots, flowers, (P =0.008 in 1993 and P = 0.001 in 1994) fruits and nuts than at Wildman River (Table 6). Lygaeidae Geocoris australis NE 23 14 Feed on Helopeltis bugs and Discussion caterpillars Weather, shelter, host and food have been observed to inf1uence insect diversity Pentatomidae (So uthwood 1978). The biological and PIaly"oplis tumer; NE 25 1 Feed on caterpillars physical factors were not significantly dif­ Reduviidae sp. NE o 11 Feed on He/opeltis nymphs ferent between the two sites (Tables 1 and Homoptera 2). Therefore, the difference in arthropod Aphididae diversity (Figure 1) between the two sites Apllis gissypii IP 155 364 Feed on new shoots, fl owers and cannot be related to the location and cli­ nuts mate. It seems likely that the understorey Coccidae of cashew trees and close contact between Ceroplastes nlbens IP 47 5 Feed on twigs and mature leaves non-crop vegetation and cashews were re­ Flatidae sponsible for the diffe rence. At the Siphmlla patrueiis IP 36 102 Feed on leaf shoots Howard Springs site, the understorey Pseudococcidae sp. IP 125 135 Feed on leaf shoots which was dominated by five species was very dense between tree rows, and the Hymenoptera cashews were closely surrounded by non­ Encyrtidae crop vegetation composed of 32 tree spe­ Encyrtinae sp. IP 142 42 Parasitize ladybird pupa cies. This provided a wide range of hosts, Aphilinidae a variety of food and favourable sanctuar­ Aphelillus sp. NE 21 8 Parasitize aphids ies for arthropods. At Wildman Rjver, Chalcididae however, there were a lmost no weed spe­ Bracllymeria sp. NE 3 11 Parasitize Penicillaria pupa cies and between weeding periods only a Ooencyrtus sp. NE 4 10 Parasitize Amblype/ta eggs small amount of grass was observed, and Tetracneminae sp. NE 1 12 Parasitize white louse scale the cl osest non-crop vegetation was 370 m ElI lophidae away from the experimental cashew trees. Tetrastichinae sp. NE 10 12 Parasitize tortricid eggs This monoculture of cashews provided Formicidae poor a lternative food sources and hosts lridomyrmex sanguinells NE 23 20 Feed on caterpillars for the arthropod community. Oecophy lJa smaragdilla NE 26 545 Feed on pest bugs, beetles and The fa rming practice of cashews can be caterpillars regarded as mono-cropping at Wildman River, but not at Howard Springs. Due to Platygasteridae the availability of alternative hosts, food Aphallomerus sp. NE 1 2 Parasitize flatids sources and sanctuaries, natural enemies Scelionidae were more abundant than insect pests Cryon sp. NE 21 20 Parasitize Amblypelta eggs each month at the Howard Springs site Trichogrammatidae sp. NE 5 9 Parasitize tortricid eggs (Table 4). However, at the Wildman River Table 3 continued on opposite page\ ... si te where alternative hosts and food Plant Protection Quarterly VoI.13(1) 1998 19 Table 3 continued. sources were very limited, natural en­ emies were generall y less abundant th an Species Status Total number Feeding habit determined by fl exible insect pests, especiall y in the most sus­ trapped at net bags and field observations ceptible period for cashews fr om pre­ WRP HS flowering flush (April) to fruiting (Octo­ ber) (Table 4). The ratio of natural enemies Lepidoptera to insect pests each month was much Geometridae higher at Howard Springs than a t AflisDzyga pieroides IP 26 5 Feed on leaves and flowers Wildman River (Table 4). This difference Gracillaridae may reflect the different periods of time Caloptilia panclirista IP 314 22 Feed on young leaves taken for various natural enemies to mi­ Noctuidae grate into the study area once pesticides Penicillaria jocosatrix IP 101 17 Feed on foliar fl uch, flowers, frui ts were withheld. In the samples of October and nuts 1994 after 15 months without pesticides, the numbers of samples containing the Tortricidae predator species O. smaragdina at Wi ld­ Adoxyphyes sp. IP 45 18 Feed on leaf shoots man River were close to those at Howard Neuroptera Springs (Table 5), which seems to support Chrysopidae the above explanation. However, other Chrysopa? sp. NE 28 17 Feed on aphids natural enemy species such as Oxyopes sp., Hemerobiidae Coelophora sp., Crypto/aemlls nlOlmtrollzieri PsycilObiella sp. NE 16 5 Feed on aphids and chalcids were much more abundant Ma llada innotata NE 5 2 Feed on mealybugs at Howard Springs than at Wildman River Mantodea (Table 3). Some natural enemies such as Mantidae Eristalis sp., Rhyzobius sp. and a species of Orthoderinae NE 8 10 Feed on Helpeltis, Amblype/ta and reduviids, only occurred at Howard moths Springs (Table 3), which supports the hy­ pothesis that there will be a greater abun- dance and diversity of natural enemies of pest insects in polycultures than in mono­ Table 4. The total number of cashew insect pests (lP) and their natural cu Itures (Root 1973). enemies (NE), the ratio of the n atural enemies to pests and the phenology of The most important predator species in the cashew plantation is 0. smaragdina, cashew trees for each month at Wildman River Plantation and Howard which can significantly reduce damage Springs. caused by the main insect pests H. Date Wildman River Howard Springs Cashew tree pernicialis, A. lutescell s and P. jocosalrix (Peng et al. 1995, in press). At the Howard NE IP Ratio NE/IP NE IP Ratio NE/IP phenology Springs site, 0. smaragdina was found in 09/93 109 71 1.54 173 64 2.70 Fruiting 50-100% of samples obtained at each sam­ 10/93 95 132 0.72 169 21 8.05 Fruiting pli ng occasion and they were abundant 12/93 52 43 1.21 73 13 5.62 Leaf flush throughout the year (Table 5). Well estab­ 01/94 81 29 2.79 80 7 11.43 Dormancy lished O. smaragdina colon ies were found 02/94 35 21 1.67 107 18 5.94 Leaf flush on most non-crop trees, and they were 03/94 52 144 0.36 200 20 10.00 Dormancy able to access th e cashew block through 04/94 24 29 0.83 84 33 2.55 Leaf flush many points of contact between non-crop 05/94 70 104 0.67 155 21 7.38 Leaf flush trees and cashews (Peng et al. in press) 06/94 91 91 1.00 182 132 1.38 Flowering once pesticides were withheld. In contrast, 07/94 124 235 0.53 172 110 1.56 Flowering at Wildman River, only a few ind ividuals 08/94 106 226 0.47 313 311 1.01 Fruiting of this important predator species were 09/94 146 253 0.58 396 133 2.98 Fruiting caught (Tables 3 and 5). Although there 10/94 115 142 0.81 300 34 8.82 Fruiting were well established O. smaragdina colo­ nies in the surrounding non-crop vegeta­ tion area, th e d istance between native trees and cashews was too far (370 m) for Table 5. The number of samples with Oecophylla smaragdina (NSOS) and O. smaragdina to walk to cashew trees (ob­ the total number of individuals of O. smaragdina (TNOS) caught in each servations done in this study). This meant sampling occasion at Wildman River Plantation (WRP) and Howard that the dispersal of O. smaragdina into the Springs (HS) from September 1993 to Odober 1994. Ten random samples Wildman River cashews mainly relied on were taken each month at each site. winged female colonization. During cashew flushing and fl owering periods Year (April- july, Table 4), the populations of Site Type 1993 1994 the major insect pests, H. pemicialis, A. llitescens and P. jocosatrix, built up quickly Sep Oct Dec jan Feb Mar Apr May jun jul Aug Sep Oct due to the lack of efficient natural preda­ WRP NSOS 0 0 1 0 0 1 1 0 0 2 1 3 6 tors. In particular, an outbreak of H. TNOS 0 0 1 0 0 1 1 0 0 2 1 4 16 pernicia/is occurred at the Wildman River site from july to September (Peng et al. HS NSOS 5 6 7 9 10 8 8 6 7 5 6 8 8 1996), and this resulted in almost no yield TNOS 12 7 39 46 49 107 20 101 31 16 17 29 71 (Table 6). 20 Plant Protection Quarterly Vo1.l3(1) 1998

Table 6. Comparison of yield per tree between two sites using group sample t tests, n = 8 trees. Yield Wildman River Howard Springs p (kg/tree ± SD) (kg/tree ± SD) 1993 0.8 ± 1.3 3.2 ± 1.6 4.57 0.008 1994 0.4 + 1.1 4.7 + 2.1 4.83 0.001 Note: Trees were eight years old at Wildman River and six years old at Howard Springs, which means the yield at Wildman River should be higher than at Howard Springs.

Co-existence between O. smaragdi lla Fisher, R.A., Corbet, A.S. and Williams, and homopterans was noted by Das (1959) C.B. (1943). The relation between the and Chen (1962). A comparison of abun­ number of species and the number of dance of insect pest species between the individuals in a random sample of an two sites showed that only homopteran animal population. /oumal of Animal insect pests were more abundant at Ecology 12, 42-58. Howard Springs than at Wildman River Houston, W. and Malipatil, M.B. (1991). (Table 3). A detailed analysis showed that Bioecology of cashew insects at although O. smaragdina co-existed with Wildman River, Northern Territory. Aphis gossypii (G lover) and a species of Research report to the Rural Industries Pseudococcidae, green ants did not affect Research and Development Corpora­ the populations of their predators tion, Canberra, Austra li a. CoeJophora sp. and Cryptolaemus mOl1t ­ Peng, R.K., Christian, K. and Gibb, K. rOllzieri (Mulsant) (Table 3) that were also (1995). The effect of the green ant, effective predators of aphids and soft Oecopllyl/a s11Iaragdina (Hymenoptera : scales of the understorey. Formicidae), on insect pests of cashew These data demonstrate that non-crop trees in Australia. Bulleli'l of E1l10mologi­ vegetation surrounding cashews and in cal Research 85, 279·84. the understorey provide habitat for ar­ Peng, KK., Christian, K. and Gibb, K. thropods that are predators and parasites (1996). The effect of native vegetation of pest species. Furthermore, trees at the on the cashew arthropod fauna with site with high ratios of predators to pests particular reference to the most impor­ had higher yield s than the trees at the site tant pest - Helopeltis pemicialis. Re­ with low ratios of predators to pests, search report to the Rural Industries which suggests that non-crop vegetation Research and Development Corpora­ adjacent to and in cashew plantations can ti on, Canberra, Australia. increase crop yield. Peng, R.K., Christian, K. and Gibb, K. (In press). Distribution of the green ant, Acknowledgmel1ts Oecophylla smaragdilla (F.) (Hymenop­ The study was supported by a Post­ tera: Formicidae), in relation to native doctoral Fellowship from the Northern vegetation and the insect pests in Territory University and a grant from the cashew plantations in Australia. Inter­ Rural Industries Research and Develop­ national/ouma/ of Pest Management. ment Corporation. We thank Wildman Root, KB. (1973). Organization of a plant­ River Plantation, Ian Duncan and Les arthropod association in simple and di­ Brigden for providing us with study sites verse habitats: The fauna of collards and necessary facilities. We also thank (Brassica oleracea). Ecological Monographs Graham Brown and Stua rt Smith for their 43,95-124. permission to use insect coll ections at the Southwood, T.KE. (1978). 'Ecological Northern Territory Museum and the methods', 2nd edition, p. 542. Northern Territory Department of Pri­ (Chapman and Hall, London). mary Industry and Fisheries. Stonedahl, G.M., Malipatil, M.B. and Hou­ ston, W. (1995). A new mirid References (Heteroptera) pest of cashew in North­ Chen, S. (1962). The oldest practice of bio· ern Australia. Bulletin of Entomological logical control: the culture and efficacy Research 85, 275·8. of Oecopliylla smaragdiua Fabr. in orange Wright, A.F. and Steward, A.j.A. (1992). A orchards. Acta Eut011l0/ogica Siuica 11, study of the efficacy of a new inexpen­ 401 -7. sive type of sucti on apparatus in quan­ Das, G.M. (1959). Observations on the as­ titative sampling of grassland sociati on of ants with coccids of tea. inveterbrate populations. Bulletin of Bulletin of Entomological Researcll 50, British Ecological Society XXIII, 116-20. 523·58.