A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): a Promising Biocontrol Agent for Bagworm Management

Oil Palm Bulletin 80 (May 2020) p. 6-14 A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): A Promising Biocontrol Agent for Bagworm Management

Siti Nurulhidayah Ahmad*; Saharul Abillah Mohamad* and Mohamed Mazmira Mohd Masri*

ABSTRACT dalam persekitaran ladang sawit. Kerosakan akibat serangga ini juga turut dilaporkan terjadi ke atas Bagworms (Lepidoptera: Psychidae) are one of the tanaman yang lain. Serangga pemangsa, Sycanus dominant defoliator pests in oil palm plantations. dichotomus Stal. (Hemiptera: Reduviidae), telah They have also been reported as pests on other crops dikenal pasti sebagai serangga yang berpotensi and on ornamental trees. A generalist predatory untuk membantu mengawal populasi ulat bug, Sycanus dichotomus Stal. (Hemiptera: bungkus secara semula jadi. Dalam kajian ini, Reduviidae), is one of the alternative means to kesesuaian pelbagai jenis mangsa sebagai sumber manage the pest naturally. In this study, the makanan S. dichotomus dinilai dari segi tempoh suitability of different types of prey as food sources perkembangan hidup serangga pemangsa. Kos for S. dichotomus was evaluated based on the pemeliharaan serangga pemangsa di makmal predator’s development duration. The cost involved turut dikira dalam kajian ini. Sumber makanan in the simple rearing system of the predator under yang berbeza menunjukkan tahap kesesuaian yang laboratory conditions was also calculated. Different berbeza. Larva Corcyra cephalonica didapati food sources exhibited different degrees of suitability, dapat mempercepatkan tempoh perkembangan for example, Corcyra cephalonica larvae pemangsa secara signifikan (P<0.01) jika significantly (P<0.01) shortened the developmental dibandingkan dengan dua jenis sumber rawatan time of the predator’s various life stages compared lain (larva Tenebrio molitor dan kombinasi larva with two other treatments (Tenebrio molitor C. cephalonica dan T. molitor), iaitu masing- larvae and a combination of C. cephalonica and T. masing sebanyak 17.5% dan 6.9%. Larva C. molitor larvae) by 17.5% and 6.9%, respectively. cephalonica menunjukkan kesesuaian yang tinggi C. cephalonica larvae alone represented a more sebagai sumber makanan pada tahap perkembangan suitable food source for the development of the first instar pertama dan kedua pemangsa. Walau and second instar nymphs. However, the combination bagaimanapun, gabungan dua jenis larva mangsa of both larvae recorded the shortest instar nymph’s memberikan tempoh perkembangan instar nimfa developmental time (95 days) and improved the yang paling singkat (95 hari) dan meningkatkan adult’s longevity (up to 69 days). The ratio of male jangka hayat pemangsa dewasa (sehingga 69 to female adult predators was higher when fed with hari). Nisbah pemangsa jantan:betina didapati T. molitor larvae and with the combination of both lebih tinggi dengan rawatan larva T. molitor dan larvae. The cost for mass rearing was approximately gabungan kedua-dua jenis larva. Kos pemeliharaan RM0.15 per individual predator, using laboratory- pemangsa secara pukal adalah RM0.15 per individu, reared prey as food sources. The results show that dengan penggunaan serangga mangsa yang this simple rearing system of S. dichotomus is easy dipelihara di makmal sebagai sumber makanan. to handle, and is cost-efficient. This will encourage Kajian mendapati bahawa sistem pemeliharaan the mass production of the predator for field release ringkas S. dichotomus di makmal adalah mudah purposes to be established in the laboratory. dikendalikan, murah serta akan menggalakkan pemeliharaan pemangsa secara pukal di makmal ABSTRAK bagi tujuan pelepasan S. dichotomus di ladang.

Ulat bungkus (Lepidoptera: Psychidae) salah satu INTRODUCTION serangga perosak pemakan daun yang dominan

Being one of the largest oil palm producers in the * Malaysian Palm Oil Board, 6, Persiaran Institusi, world, Malaysia has 55.81 million hectares of oil Bandar Baru Bangi, 43000 Kajang, Selangor, Malaysia. palm, from which the average fresh fruit bunch E-mail: [email protected] (FFB) yield has steadily increased to 17.19 t ha-1

6 A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): A Promising Biocontrol Agent for Bagworm Management yr-1 in 2019 (Parveez et al., 2020). Bagworms (Metisa S. dichotomus is commonly found attacking plana and Pteroma pendula) and nettle caterpillars bagworms and nettle caterpillars in oil palm (Darna spp. and Setora nitens) are the primary leaf- plantations, and is active during sunny days defoliating insect pests of oil palm in Malaysia (Zulkefli et al., 2004; Jamian et al., 2017; Siti (Norman et al., 2017). Bagworm outbreaks damage Nurulhidayah et al., 2017). They are easily found the oil palm leaves, leading to severe crop losses in oil palm surroundings (Norman et al., 2017), and (Basri, 1993). It is well understood that when have been recognised as one of the vital predators there is a breakdown in natural control, pest of bagworms (De Chenon et al., 1990). S. dichotomus numbers will increase and lead to an outbreak. has been reported as a suitable candidate for mass Integrated pest management (IPM) is the best way rearing (Wood, 1976; De Chenon et al., 1990). The to minimise the attacks by insect pests such as life cycle duration of this predator can reach 200- bagworms, as well to reduce economic losses with 249 days (Zulkefliet al., 2004; Siti Nurulhidayah and less dependency on chemical pesticides in oil palm Norman, 2016), depending on the food sources. The plantations. The utilisation of biocontrol agents ability of S. dichotomus to attack the larval and pupal such as predatory insects is one of the components stages of the bagworms makes it the best choice as in IPM. IPM components comprise beneficial plants a biological control agent (Norman et al., 2017). S. for sustaining parasitoids and predators (Norman dichotomus has an adequately long proboscis which and Othman, 2016; Siti Nurulhidayah et al., 2017), can penetrate the bag of the bagworm (Zulkefliet al., pheromone trapping, and application of biological 2004). Previous studies reported that S. dichotomus insecticides (Mohd Najib et al., 2017). can be successfully raised to develop and reproduce, using Lepidopteran and Coleopteran larvae such as Predator-prey studies have contributed Plutella xylostella (Lepidoptera: Plutellidae), Tenebrio significantly to landscape ecology and behavioural molitor (Lepidoptera: Tenebrionidae) and Corcyra science, leading to recognition of the indirect cephalonica (Lepidoptera: Pyralidae) (Zulkefli et al., interactions between predators and prey that 2004; Siti Nurulhidayah and Norman, 2016). Thus, S. dichotomus can influence the demography of the prey and had been identified as a potential predator of Metisa plana and Pteroma pendula (Jamian community interactions, as well as direct mortality et al., 2011; Yusof and Fairuz, 2011; Siti Nurulhidayah of prey (Laundré et al., 2014). The most common et al., 2020). Several studies on Sycanus species predator species found in Malaysia are Sycanus which include investigations into their field release dichotomus and Cosmolestes picticeps (Hemiptera: (Budi et al., 2008), life cycle (Zulkefliet al., 2004), and Reduviidae), Cantheconidia furcellata (Hemiptera: prey-predator relationship (Jamian et al., 2011) have Pentatomidae) and Callimerusarcufer beetle been carried out. However, data on assessing the (Coleoptera: Cleridae) (Wood and Norman, suitability of alternative prey and costs involved for 2019). Most of the assassin bugs (Reduviidae) are developing a systematic mass-rearing procedure generalist insect predators with a wide-ranging aimed at release purposes are still lacking. variety of prey (Chandra et al., 2014). The Sycanus species is also a generalist predator that has a broad Food source may be a limiting factor in range of target prey. Its target prey includes several effective predation by S. dichotomus when used as orders of insects, such as the larvae and pupae of a biocontrol agent. Thus, evaluation of alternative Lepidoptera, Diptera and Coleoptera (Sahayaraj prey species is essential to measure the quality of and Balasubramanian, 2016). Earlier studies the available food. Food quality may influence have shown that reduviid predators such as S. the growth and development of the predator, and sichuanensis Hsiao (Liu et al., 2012) and Cosmolestes this information can be beneficial in future mass picticeps Stal (Jamian et al., 2017) are suitable as rearing. Thus, the objectives of this study were to biological control agents for the nymphal and larval evaluate the suitability of alternative prey species stages of insect pests. To date, the bionomics and as food sources for S. dichotomus, and to estimate the use of other Sycanus species for biological control cost for an optimised mass-rearing system. have been reported, such as S. annulicornis for Setothosea asigna (Sahid et al., 2018), S. indigator for MATERIALS AND METHODS Galleria mellonella and Spodoptera frugiperda (Bass and Shepard, 1974), S. affinis for lepidopteran larvae The study was conducted at the Entomology in coconut groves (Satpathy et al., 1975), S. reclinatus and Ecology Laboratory, Malaysian Palm Oil for Earias insulana, E. vitelli, Heliothis armigera, Board, Bandar Baru Bangi, in Selangor. All insect- Spodoptera litura and Dysdercus cingulatus (Vennison rearing activity and experiments were conducted and Ambrose, 1992), S. macracanthus for Mahasena in a controlled environment with the following corbetti and S. asigna (Tiong, 1996), S. versicolor for conditions: day temperature (27±1°C), night H. armigera and E. insulana (Kumaraswami and temperature (24±1°C), photoperiod of 12:12 (L:D) hr, Ambrose, 1992), and S. aurantiacus for Crocidolomia and 50%-70% RH monitored by a hygrothermograph pavonana and Plutella xylostella (Ishikawa et al., 2007; (Dickson brand) (Siti Nurulhidayah and Norman, Yuliadhi et al., 2015). 2016).

7 Oil Palm Bulletin 80

The parent population of the predator, S. from Universiti Putra Malaysia, Serdang, Selangor. dichotomus, was collected from oil palm plantations A colony of C. cephalonica was reared on corn and in Teluk Intan and Tapah, Perak, and maintained in rice in a plastic rearing container (measuring 25 the laboratory. The adults were paired and caged cm x 35 cm x 12 cm). Both cereals were ground in a transparent cylindrical container (measuring separately. The ratio of corn to the rice used was 12.5 cm in diameter and 23.5 cm in height) with a 1:2, and the mixture was autoclaved at 121°C for ventilated lid. Oil palm leaflets and small ferns were 20 min. As before, the live larvae of C. cephalonica provided in the rearing container for egg-laying, and were used as the food source for S. dichotomus. Both to simulate their natural concealed microhabitat. prey (C. cephalonica and T. molitor) were chosen as Oil palm leaflets were cut and introduced through food sources because they are easily available in the a hole in the transparent plastic lid of a glass vial market, are easy to rear, and require only simple containing water to ensure their freshness and put maintenance in the laboratory. in the container. The adults were fed daily with the mealworm, T. molitor, larvae as the food source, and The effects of T. molitor larvae, C. cephalonica provided with 10% diluted honey solution in a wet larvae and a combination of both larvae on the life cotton ball. Bagworms were also supplied when duration of S. dichotomus individuals were evaluated available. These containers were examined daily for separately under the same rearing conditions. The the occurrence of oviposition and for egg collection. suitability of the food sources for S. dichotomus was The newly laid eggs were transferred carefully to a evaluated by measuring the developmental time of petri dish, and monitored until they hatched. The the predator for all stages, after moulting until the newly emerged instar nymphs were used for this next life stage. study. The pre-imaginal developmental time was The mealworm, T. molitor, (Figure 1) was estimated by observing the S. dichotomus individuals obtained from a local aquarium fish shop, and daily, from the first instar nymph to the emergence reared on sliced bread and oat bran in a transparent of the adult. Initially, the newly hatched instar rearing container (measuring 20 cm x 10 cm x 12 nymphs were transferred with a soft brush from cm), while the adults were reared on oat bran and the petri dish, and placed individually in separate sliced fresh potato in a different container. The small plastic cups (measuring 6 cm diameter x 4.5 early live larvae of T. molitor were used as the food cm height). The nymphs were assigned to either T. source for S. dichotomus. The parent population of molitor larvae, C. cephalonica larvae, or a combination the rice moth, C. cephalonica, (Figure 2) was obtained of both larvae provided as the food source. A 10% honey solution was also provided in each cage. After moulting to the third instar, the nymphs were each transferred to a larger individual transparent cylindrical cage (measuring 12.5 cm diameter x 23.5 cm height) with a ventilated lid. The live insect larvae which had been consumed were replenished at two-day intervals. The duration between each moulting was used as a basis to calculate the developmental time for each instar nymph of S. dichotomus. The life span of the S. dichotomus adult was determined from the time of its emergence until its death.

Figure 1. Mealworm, T. molitor, larvae. To evaluate the longevity of the adults, each newly emerged adult S. dichotomus was placed in an individual transparent cylindrical cage (measuring 12.5 cm diameter x 23.5 cm height) with a ventilated lid. Each adult was observed at two-day intervals to record its longevity.

The gender of S. dichotomus can only be determined after the emergence of the adult stage. The main difference between the male and female S. dichotomus is the shape of the abdomen. Jamian et al. (2011) reported that the adult female has a V-shaped abdomen while the male has a U-shaped abdomen. The female is also generally bigger and Figure 2. Rice moth, C. cephalonica, larvae. her abdomen is wider compared with the male. The

8 A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): A Promising Biocontrol Agent for Bagworm Management sex ratio was determined from the adults which It may be observed that the longest duration emerged for all the treatments. in survival within the whole life span was during the adult stage. The results show that food source RESULTS AND DISCUSSION influenced adult longevity. The adult life span was significantly longer when the predator was fed with Prey Suitability and Developmental Time of the combination of both larvae as the food source S. dichotomus (69.4 days) or with C. cephalonica larvae alone (66 days), and was shorter when fed with T. molitor In this study, all the three food source treatments larva alone (56 days) (Figure 3) (Table 1). A longer supported the development of S. dichotomus, but adult life span means it will feasibly enhance the resulted in different developmental time. The predation ability of the predator at its adult stage. total instar nymph duration for S. dichotomus fed Several studies have shown that food quality on a combination of both larvae (95 days) was affects the developmental time and survival of significantly shorter (P<0.01) compared with several predators (Kalushkov, 1998; Isıkber and feeding with T. molitor larvae alone (115 days) and Copland, 2002; Kalushkov and Hodek, 2004), as with C. cephalonica larvae alone (98 days), by 21.3% well as affects the reproductive performance of and 2.8%, respectively (Table 2). The mean life span the adults. In contrast, according to Vivan et al. of S. dichotomus fed on C. cephalonica larvae was (2003), the prolonged developmental time has significantly shorter (P<0.05) at 154 days, whereas been observed to be an undesirable characteristic S. dichotomus fed on T. molitor and a combination of both larvae lived significantly longer at 181 and 164 days, respectively. Nevertheless, T. molitor larvae ranked second in suitability because the duration during the fifth instar nymph stage was the longest, resulting in an overall slower rate in the predator’s developmental time, which extended its life span (Table 1). However, C. cephalonica larvae may be a preferred diet for the first and second instar nymph stages. It was observed that the early instar nymphs readily consumed C. cephalonica because the outer skin of the larvae is silky soft and easy to be penetrated by the younger predator unlike the skin of the T. molitor larvae. Figure 3. Adult S. dichotomus feeding on a T. molitor larva.

TABLE 1. DEVELOPMENTAL TIME IN DAYS (mean ± S.E.) OF S. dichotomus FED ON T. molitor LARVAE, C. cephalonica LARVAE AND A COMBINATION OF BOTH LARVAE

Food source Combination (T. Tenebrio molitor Corcyra Significance Stage molitor and C. larvae cephalonica larvae level cephalonica larvae) (days) (days) (days) 1st instar 19±0.62a 15.2±0.44b 18±0.47a ** nymph 2nd instar 17.8±1.04a 13.9±0.50b 15.2±0.39b ** nymph 3rd instar 20.7±0.45a 18.2±0.8b 16.6±0.88b ** nymph 4th instar 25.4±0.72a 21.3±0.45b 20.6±0.85b ** nymph 5th instar 32.2±0.77a 29±0.6b 24.5±0.81c ** nymph Adult 65.5±2.38a 56.1±1.8b 69.4±2.41a ** Total 180.6±8.31a 153.7±2.31b 164.3±6.83ab *

Note: ** - significant at P<0.01. * - significant at P<0.05. Values bearing different letters within a row are significantly different from one another.

9 Oil Palm Bulletin 80 under field conditions, because it causes a lower Generally, the experiments revealed that food predator population growth rate, a lower number source suitability for S. dichotomus depended on of generations per year, and therefore reduced the type of prey larvae and also whether they biocontrol efficiency. were fed as a mixture. Similar results have been reported in studies on other generalist predators, It has been observed that S. dichotomus fed such as Coccinella undecimpunctata (Coleoptera: with the combination of both insect larvae was Coccinellidae) and Clitostethus arcuatus (Coleoptera: significantly bigger in body size, with adults Coccinellidae) (Cabral et al., 2006; Yazdani and living considerably longer and healthier (Siti Zarabi, 2011). Nutritional value might differ among Nurulhidayah and Norman, 2016). ElHag and the prey species. O’Neil and Wiedenmann (1990) Zaitoon (1996) also observed higher survival reported that in their study on the insect predator, rates of Coccinella undecimpunctata (61.5%) when Podisus maculiventris, the predator maintained they used a mixed diet of two aphids, Brevicoryne its reproductive output and weight only when brassicae and Rhopalosipum padi (Homoptera: it had abundant prey. Reproduction can also be Aphididae). According to Vivan et al. (2003), the 5th maintained on a diet of small prey, indicating the nymphal instar of the stinkbug Podisus nigrispinus capacity for proficient extraction of nutrients and (Heteroptera: Pentatomidae) showed enhanced flexible foraging (Mills, 1982). The presence of low- development of the reproductive organs, thus the quality prey species may, therefore, counteract the higher food quality of the combination of the two benefits of mixed food sources for the predators. larval types may also affect the adult growth of S. Performance, in terms of the parameters measured, dichotomus. was better when the predators were fed a mixture of prey compared with a single prey, especially during Longevity and Sex Ratio of S. dichotomus the nymphal instar development stages.

The sex ratio among all the treatments was also It was also observed that the development time observed (Figure 4). The male to female sex ratio of the first and second instar nymphs ofS. dichotomus was higher (6:4 and 7:3, respectively) in treatments was much longer when fed with T. molitor larvae in which S. dichotomus was fed with T. molitor larvae compared with the other food source treatments alone and with a combination of both larvae, while (Table 1). This was possibly due to the inability of the female to male sex ratio was higher (9:1) when the young nymphs to penetrate the cuticle of the T. they were fed with only C. cephalonica larvae. In molitor larvae with their rostrum. In the combined all the treatments, the life span for females was larvae treatment, it was observed that the first always longer than for males. A similar pattern and second instar nymphs preferred consuming was also observed in an earlier study conducted by C. cephalonica larvae rather than T. molitor larvae. Srikumar et al. (2014). He reported a longer life span In terms of developmental time, S. dichotomus fed for females than for males as a common feature of with C. cephalonica recorded a relatively shorter life most reduviids. span. Thus, it can be concluded that C. cephalonica

100 90 80 70 60 50 Male

Gender (%) 40 30 Female 20 10 0 T. molitor Combination of C. cephalonica both larvae Food sources

Figure 4. Sex ratio of S. dichotomus fed different food sources.

10 A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): A Promising Biocontrol Agent for Bagworm Management larvae were the preferred prey for the early instar throughout the nymphal development stages as nymphs of S. dichotomus. The suitability of different well as for the maintenance of the adult. prey types as food sources for the predators can be diverse. Many predatory insects appear to Thus, the cost for mass rearing the predator, S. be opportunistic in the field, feeding on a wide dichotomus, was reduced by 76%, from RM0.63 to range of prey species, but this behaviour may not RM0.15 per individual by supplying reared prey indicate prey suitability and predator nutritional to the predator (Siti Nurulhidayah et al., 2011). requirements (Thompson, 1951; Thompson and Mixed prey seems to be the ideal food source for Hagen, 1999). Predator diet specificity, feeding enhancing the growth and development of the preference and capacity for population increase are predator and for promoting healthy adults. Overall, the factors that largely depend on prey suitability it is economically feasible to rear the prey rather (Dixon, 2000). than to purchase them, and these reared prey are suitable as a food source to be used in the mass According to Symondson et al. (2002), generalist rearing of S. dichotomus. predators are polyphagous and can maintain their population on a wide range of alternative TABLE 2. ESTIMATED COST (RM) OF LIVE PREY prey when any single pest species is absent. In agricultural systems, alternative prey may improve Estimated the generalist predators’ survival when the target Cost per Cost per No. of pests are occasional in occurrence (Ehler and Miller, Prey individual kg (rm) larvae 1978; Eubanks and Denno, 2000). Thus, alternative prey (Rm) (per kg) prey should be beneficial from the predator’s perspective. Similarly, McMurtry (1992) revealed T. molitor 52.80 12,886 0.004097 that the generalist phytoseiids (Mesostigmata: (commercial) Phytoseiidae) are frequently observed for long T. molitor 4.70 12,886 0.000365 periods on plants in the absence of prey, and feed (reared) on alternative food. Factors such as a long life cycle, C. cephalonica 18.10 36,764 0.000493 quality of parent colonies, decline in fecundity, (reared) inbreeding, high cost of production and lack of expertise should be carefully considered before Source: Siti Nurulhidayah et al. (2011). pursuing laboratory rearing of the predator.

However, the developmental and reproductive CONCLUSION performance of S. dichotomus fed on the alternative prey as food sources need to be assessed over S. dichotomus was successfully reared into healthy subsequent generations. The reason is that any and fecund adults in the laboratory using live nutritional imbalances within the diet will possibly reared prey as food sources. The observations on be expressed only in the subsequent generations the developmental time of each life stage of the (De Clercq et al., 2005), as has also been suggested predator, as well as on the longevity and gender of by Nguyen et al. (2013) with reference to their study adults, fed with live larvae of T. molitor, C. cephalonica on the predatory mite, Amblyseius swirskii. and a combination of both larvae, allowed for evaluation of the suitability of the food sources. The Cost of Prey Production as Food Source findings show that the growth and development of S. dichotomus was enhanced if reared using a Mass rearing of predators for release poses combination of both larvae as the food source, many challenges, such as the cost of maintaining rather than using the larvae of each single prey insect-prey cultures (Grundy et al., 2000) and the species, especially during nymphal instar stages. risk of prey scarcity due to mismanagement of the Thus, the diet comprising a combination of both facilities or disease (De Clercq and Degheele, 1992). larvae is more suitable to be used as one of the food Thus, a comparison of the estimated cost of rearing sources in a S. dichotomus mass-rearing system. prey and the price of commercially available prey The low cost for mass rearing of S. dichotomus was made as shown in Table 2. At approximately (approximately RM0.15 per individual) supplied RM0.15 per predator, it is economically viable with reared prey showed high potential in using the to raise the predator on live prey reared in the artificially reared predator as one of the components laboratory (Table 3), because this is 76% lower in the IPM system. These findings can serve as compared with commercially available prey (at a guide to develop a more feasible mass-rearing RM0.63 per predator). The total cost of producing protocol in future. However, in order to release the one S. dichotomus adult was calculated based on predatory insects as a biological control agent in oil prey preference, as shown in Table 3. The cost was palm plantations, the maintenance of local habitat also based on the number of live prey consumed complexity and farmland biodiversity is crucial. 11 Oil Palm Bulletin 80

TABLE 3. ESTIMATED TOTAL COST (RM) TO PRODUCE ONE S. dichotomus ADULT BASED ON REARED PREY

No. of prey consumed Cost per Estimated life Feeding stage (per day) individual span (days) C. cephalonica T. molitor (Rm) 1st and 2nd instar nymphs 30-40 2 0 0.033 3rd to 5th instar nymphs 60-80 1 1 0.053 Adult 60-70 1 1 0.059 Total cost 0.145

Source: Siti Nurulhidayah et al. (2011). Note: The cost did not include labour cost.

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12 A Simple Laboratory System for Rearing of the Predator, Sycanus Dichotomus (Hemiptera: Reduviidae): A Promising Biocontrol Agent for Bagworm Management

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