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Diet-Dependent Fecundity of the Spiders Atypena Formosana and Pardosa Pseudoannulata, Predators in Irrigated Rice

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Diet-Dependent Fecundity of the Spiders Atypena Formosana and Pardosa Pseudoannulata, Predators in Irrigated Rice Agricultural and Forest Entomology (2001) 3, 285±295 Diet-dependent fecundity of the spiders Atypena formosana and Pardosa pseudoannulata, predators in irrigated rice Lene Sigsgaard*, Sùren Toft² and Sylvia Villareal* *International Rice Research Institute, PO Box 3127 (MCPO), 1271 Makati City, Philippines and ²University of Aarhus, Department of Zoology, Bldg. 135, DK-8000 Aarhus C, Denmark Abstract 1 The fecundity of the spiders Atypena formosana and Pardosa pseudoannulata was assessed on diets of brown planthopper Nilaparvata lugens (BPH), green leafhopper Nephotettix virescens (GLH), Collembola (Entomobryidae), Droso- phila melanogaster and three prey mixtures; BPH±GLH, BPH±GLH±Collembola and a full mixed diet of BPH±GLH±Collembola±D. melanogaster. 2 Egg production and hatching success was high in A. formosana except on the BPH, the GLH and the BPH±GLH diets. In P. pseudoannulata egg production and hatching success was lowest on diets of GLH and BPH±GLH, whereas this spider used BPH better. 3 Differences between offspring sizes were small. 4 Survival of A. formosana females was lowest on the GLH and BPH±GLH diets. In P. pseudoannulata survival did not differ signi®cantly. 5 Food conversion ef®ciency was highest on the Collembola and the D. melano- gaster diets for both spiders. 6 Overall, diets of Collembola and D. melanogaster had the highest quality for both spiders, the BPH±GLH±Collembola and the full mixed diets were intermedi- ate in quality, the quality of the BPH diet was intermediate to low and quality of the GLH and BPH±GLH diets was low. 7 There need not be a contradiction between low dietary value of hoppers and suc- cessful natural biological control provided that the nutritional needs of the spiders are met by suf®cient alternative prey. 8 The hopper-spider relationship is comparable to that of aphids and spiders in temperate cereals, suggesting that low dietary quality of Homopterans to spiders may be widespread. Keywords Atypena formosana, biological control, Collembola, Drosophila melanogaster, fecundity, Nephotettix virescens, Nilaparvata lugens, Pardosa pseudoannulata, spider, prey. dominant spiders in the ®rst 35±40 days after transplanting. Introduction Together with Tetragnatha spp., they are the most abundant Spiders are an important part of the natural enemy complex that spiders across the rice-cropping season (Barrion & Litsinger, normally keeps insect pests in check in unsprayed, irrigated rice 1984; Heong et al., 1992). Atypena formosana lives among the (Matteson, 2000). In the Philippines, the money spider Atypena rice tillers at the base of rice hills. It hunts for nymphs of formosana (Oi) (Linyphiidae) and the wolf spider Pardosa planthoppers and leafhoppers, Collembola and small dipterans. pseudoannulata (Bosenberg & Strand) (Lycosidae) are the The web is a sheet web or an irregular web of about 8 cm in diameter, placed 0±20 cm above the ground. In the webs, 36% of the prey is Homoptera and 57% Collembola (Barrion, 1999). Correspondence: L. Sigsgaard, Royal Veterinary and Agricultural University, Department of Ecology, The Zoology Section, Pardosa pseudoannulata spins no web but hunts most Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark. Tel.: commonly among the tillers at the base of the plants (Ooi & +45 35282668; fax: +45 35282670; e-mail: [email protected] Shepard, 1994; Barrion, 1999). ã 2001 Blackwell Science Ltd 286 Lene Sigsgaard et al. Pardosa pseudoannulata is recognized as a signi®cant (Gavarra & Raros, 1975) and P. pseudoannulata prefer biological control agent of insect pests in irrigated rice. It can Collembola to Sogatella furcifera (Pang et al., 1998). effectively regulate the pest population of leafhoppers and Drosophila melanogaster has been recognized as a high-quality planthoppers, and is perhaps the single most important predator diet for money spiders and wolf spiders, the quality to some of brown planthopper (BPH) Nilaparvata lugens StaÊl extent dependent on the substrate offered to D. melanogaster (Hemiptera: Delphacidae) (Kiritani et al., 1972; Kobayashi & (Mayntz & Toft, 2001). Food value depends on the energy and Shibata, 1973; Kiritani & Kakiya, 1975; Kenmore et al., 1984; nutrient content of a prey, sometimes interacting with deterrents Ooi & Shepard, 1994). Reports of the importance of A. or toxins. It may be expressed by a ®tness estimate for the formosana are more recent (Reddy & Heong, 1991; Barrion, predator combined with measurement of the feeding rate. Egg 1999). High predation rates demonstrate that both spiders have production, hatching success, size of offspring, food conversion the potential to control populations of BPH and Nephotettix ef®ciency (eggs produced per mg diet) and female survival were virescens (Distant) (Hemiptera: Cicadellidae) (GLH) (Heong & used as ®tness parameters for evaluating the food quality of Rubia, 1989; Heong et al., 1991; Sigsgaard & Villareal, 1999). BPH, GLH, Collembola, D. melanogaster and mixed diets for A high density of spiders in the ®eld early in the cropping A. formosana and P. pseudoannulata. We tested the hypothesis season can probably contribute signi®cantly to a reduction in the that, due to differences in food quality, these diets would number of BPH and GLH (Kenmore et al., 1984; Settle et al., differentially affect the reproduction of spiders. Prey quality 1996). A community of alternative prey would help to support may not affect initial acceptance because prey rejection is an such a high density of spiders in the ®eld (Wu et al., 1994; Guo acquired response (Toft, 1995; Toft & Wise, 1999a, b). et al., 1995; Settle et al., 1996). In Japan, releases of D. melano- However, prey quality will affect subsequent predation rates gaster in dikes surrounding a rice ®eld prior to transplanting and spider ®tness in terms of number of offspring (numerical signi®cantly increased the control of two hoppers, Nephotettix response) and survival and development of spiderlings. cincticeps and Laodelphax striatellus, illustrating the impor- Therefore, it is likely to affect the diet composition eaten by tance of abundant prey in the fallow (Kobayashi, 1975). the spider over a longer time span. Spiders are generalist predators and can potentially add to the control of a variety of insect pests (Riechert & Luczak, 1982; Materials and methods Riechert & Lockley, 1984; DeKeer & Malfait, 1988; Axelsen et al., 1997; Sunderland et al., 1997). However, spiders are Spiders affected by prey quality, which in turn may affect their effectiveness as natural enemies. Thus, the money spider To obtain adult female spiders of the same age for the Erigone atra has a limited ability to prey on the cereal aphid experiment, late-instar A. formosana and P. pseudoannulata Rhopalosiphum padi (Toft, 1995), its offspring are smaller on were ®eld-collected in Laguna province, the Philippines, and pure aphid diets than on aphid±D. melanogaster diets (Bilde & reared on excess of a mixed diet of BPH, GLH, Collembola and Toft, 2001), and Alderweireldt (1994) observed that a large D. melanogaster until they became adults. Spiders were proportion of the aphids caught in the webs of money spiders collected over a month and adults developed over a period of were not consumed. We demonstrated that young A. formosana 6±7 weeks. Spiders that became adults were assigned treatments were unable to develop to maturity on diets of BPH or GLH, in turn, so that the time spread in treatments was equal. There was whereas Collembola were high-quality prey (Sigsgaard et al., no statistically signi®cant difference in female initial weight 2001). Thang et al. (1988) found faster development of P. among treatments. pseudoannulata on a mixture of BPH nymphs and D. melanogaster larvae than on a pure diet of either. Suzuki & Prey species Kiritani (1974) showed that its fecundity was higher on mixed prey than on the leafhopper N. cincticeps alone. Finally, All cultures were established from arthropods collected in survival of spiderlings of Pardosa amentata was signi®cantly Laguna Province, the Philippines. Cultures of BPH and GLH poorer on diets of aphids than on diets of D. melanogaster or were maintained in insect cages in the greenhouse following the Collembola (Toft, 1995). procedure described in Heinrichs et al. (1985). Young second- The dietary value of an alternative prey determines its role in instar nymphs of GLH and BPH were used as prey for A. maintaining a high population of A. formosana and P. formosana and ®fth instars for P. pseudoannulata. A D. pseudoannulata early in the cropping season. Thus, we designed melanogaster culture was established by collecting adults from an experiment to assess the dietary quality of the most common ripe banana. The culture was maintained on ripe banana in test prey in irrigated rice, represented by BPH for planthoppers, tubes in the greenhouse. Ten adults were put in a test tube with GLH for leafhoppers, D. melanogaster Meigen (Diptera: ripe banana for 24 h for oviposition. Newly emerged adults were Drosophilidae) for ¯ies and Collembola (Entomobryidae). used for spider food. Collembola were ®eld-collected. We used a Drosophila melanogaster is known as a valuable food source mixture of Collembola from the family Entomobryidae, which (Toft, 1995) and the importance of Collembola to money spiders was the predominant collembolan family in ®eld collections. seems to be general for cereal ®elds in temperate regions (Chiverton, 1986; Sunderland et al., 1986; Nyffeler, 1999). Experimental conditions Evidence suggests that this may also be true in Asian rice ®elds (Settle et al., 1996; Barrion, 1999; Sigsgaard et al., 2001). One male and one female A. formosana were kept as a pair in test Collembola are important for immature P. pseudoannulata tube vials 180 mm long and 15 mm in diameter, closed with a ã 2001 Blackwell Science Ltd, Agricultural and Forest Entomology, 3, 285±295 Diet-dependent fecundity of two spiders in rice 287 moist cotton plug in ®ne nylon mesh. Under these conditions, females readily produced egg sacs. After oviposition, the two adult spiders were moved to a new vial.
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