Systematic & lied ~carnlo& (2003) 8.67-74. ISSN 1362-1971 Studies on the life history of Amblyseius cucumeris (Acari: Phytoseiidae) feeding on Aponychus corpuzae (Acari: Tetranychidae) YANXUAN ZHANG', JIANZHEN LIN', ZHI-QIANG ZHANG~, YUTAKA SAITO~ & JIE JI ' ' Institute of Plant Pro~ection, Fujian Academy of Aricullural Science, Fuzhou 350013, China Landcare Research, Private Bag 92170, Auckland, New Zealand Laboratory of Animal Ecology, Department of Ecology and Systematic, Graduate School ofagiculture, Hokkaido University, Japan Abstract This laboratory study examines the life history of Amhly.veius cucumeris feeding on Aponychus corpuzae under four constant temperatures. The females of Amhlyseius cucumeris required 20.0a.5 days to complete its development from the egg to adult at 15± 'C, but only 7.7b0.3 days at 30±1 The developmental duration of each stage of A. cucumeris decreased with increasing temperature from 15'C to 30 C The average oviposition period was 22.2b1.6 days, and the fecundity was 28.9±1. eggs. The female longevity (egg to death) was 40.64C0.7 days. Latoratory studies of predator : prey numerical responses revealed that at the ratios between 3 : 30 and 9 : 30, predators quickly brought A. corpuzae populations under control and the prey densities began to decrease from the 4th days after predator introduction. The present study shows that A. cucumeris can develop, survive and increase its population when feeding on A. corpuzae and has good potential as a biological control agent of A. corpuzae in moso bamboo forests in Fujian, China. Key words: Amh1y.veiu.v mcumeris (Oudernans), Aponychus cotpuzae (Rimando), life history, biological control, predator-prey interaction Introduction - The spider mite Aponychus corpuzae (Rimando) is a widespread species that occurs on a variety of bamboo species in the world (Holland et al. 1998). It was first reported as a major pest species on the moso bamboo (Phyllostachys puhescens) in Zhejiang Province, China (Yu & Shi 1991). In Fujian this species is also a major pest on the moso bamboo (Zhang et dl. 1997). It is much more common and widespread than other spider mite species on moso bamboo. In Fujian bamboo forests, Typhlodromus hamhusae Ehara is a dominant natural enemy of Schizotetranychus nanjingensis Ma & Yan and other phytophagous mites (Zhang et at. 2000b). However, its density is not enough to suppress S. nanjingensis, Aponychus corpuzae, S. hamhusae Reck and Aculus hamhusae Kuang, especially in the bamboo growing season. Furthermore, T. hambusae as well as some other phytoseiids occurring on bamboo are not always effective in controlling other phytophagous mite pests, and pest mite outbreaks occur sometimes in Fujian, China (Zhang et at. 1997, 2000b). Therefore we searched for some predatory mites which can be massproduced in an easier and cheaper way. The predatory mite Amhlyseius cucumeris (Oudemans), sometimes cited by some authors in literature as Neoseiulus cucumeris, is such a predator. It has been used widely as a biological control agent for regulating various species of thrips rather than 0 2003 Systematic &Applied Acarology Society 67
mites, although it also feeds on mites (Gerson et al. 2003). The effects ofa. cucumeris on mites are not well known and the limited number of reports showed that the results are variable. Amblyseius cucwneris failed to reproduce when feeding on an eriophyid mite, Aculops lycopersici (Massee) (Brodeur et at. 1997), but it was effective against the cyclamen mite, Phytonemus pallidus (Banks) on strawberries (Croft et al. 1998; Tuovinen 2000,2002) and the broad mite, Polyphagotarsonemus latus (Banks) on greenhouse plants in China (L. R. Liang, personal communication). Both species are members of the Tarsonemidae. Amblyseius cucumeris feeds on spider mites but has rarely been considered for use to control these mites. We were the first to report on the potential of A. cucumeris against 5'. nanjingensis (Zhang et al. 2000a). In this study, we examined the potential of A. cucumeris against A. corpuzae., Materials and methods Mites and plants The predatory mite A. cucumeris originated from a colony in the Biological Crop Protection Limited in England and was reared on Tyrophugus putrescentiae (Schrank) in the laboratory. Aponychus corpuzae used in this study originated from the moso bamboo in Gongchuan Village, Yongan county, Fujian province, China. The leaves of moso bamboo were collected from bamboo forests in Nanping country, Fujian. Leaves not immediately used were stored in plastic bags at 5OC. General description of the experimental setup Petri dishes (diameter 6 or 12 cm) were used as platforms for rearing and observing mites (see Zhang et al. 1998 for details). Bamboo leaves were placed on a piece of filter paper, which rested on a piece of foam plastic soaked with water in a Petri dish. Leaves were replaced every five days by placing a fresh leaf close to the old leaf. When the mites moved to the new leaf, the old leaf was discarded. Development An egg of the predatory mite was transferred to a clean bamboo leaf. The development of the egg was observed at 12-hour intervals until it reached adulthood. The predatory mites were fed an abundance of A. corpuzae. The experiments were conducted under 15±1 20±1 25±1 30±1 15L : 9D and 70-80% RH conditions. Reproduction A newly mated A. cucumeris female was introduced onto a detached leaf (2 x 2 cm) of green bamboo (Dendrocalamus latiflorus) and was fed sufficient numbers of females and eggs of A. corpuaze. The oviposition of the predator female was checked daily and the eggs laid were removed after the observation. The observations were continued until the predators stopped oviposition or died. There were 10-30 replicates. The experiments were conducted in controlled condition growth chambers at 25±1 15L : 9D and 70-80% RH. Response to predator density Petri dishes (diameter 6 cm), each with a water-soaked foam plastic (diameter 4 cm) inside, were used as observation units. The water-soaked foam plastic was covered with a detached leaf (2 x 2 cm) of green bamboo (Dendrocalamus fatiflorus). The number of A. corpuzae provided was 30 females per disk. Then 1,3,5,7 or 9 predator females ofa. cucumeris were introduced into the unit. SYSTEMATIC & APPLIED ACAROLOGY VOL. 8
There were five replicates per predator density. All experiments were conducted in growth chambers controlled under 25±1 and 15L : 9D and 70-80% RH conditions. Result and analyses Life history of A. cucumeris feeding on A. corpuzae at 4 constant temperatures The present experiment showed that A. cucumeris could feed on every stage of A. corpuzae, and preferred active stages to eggs of the prey. TABLE 1. Developmental period of each stage in days (MeanGE) ofa. cucumeris feeding on the A. corpuzae under 4 constant temperatures conditions. Sex N Egg Larva Protonymph Deutonymph Preoviposition Egg-egg 15+1 F 30 5.150.2 2.39.5 3.320.6 4.450.5 4.920.7 20.w.5 M 20 5.220.2 2.3k0.4 3.320.4 4.320.4 15.Q0.4 20+lnC F 16 4.79.7 1.3k0.5 2.3k0.5 2.39.5 2.4i1.6 12.9H.2 M 10 4.620.6 1.340.4 2.1k0.3 2.79.5 --- 10.7M.4 25+1 F 25 2.520.6 1.09.4 1.520.7 2.19.4 2.520.6 9.6k0.6 M 17 2.620.5 0.9N.3 1.720.5 2.29.1 7.320.4 30+1 F 19 2.1k0.4 0.8i0.2 1.350.2 1.6+0.2 1.9i0.5 7.7i0.3 M 17 2.0k0.3 0.89.1 1.3k0.2 1.89.2 5.820.2 Females ofa. cucumeris required 2W0.5 days to complete its development from the egg to adult at 15±1 but only 7.7k0.3 days at 30±1 (Table 1). The duration of each stage decreased with increasing temperature from lsâ to 30 C The relationship between temperatures (X) and development period of each stage (Y) of female of A. cueurneris could be fitted to the linear equation as follows: The relationship between temperatures (A') and development period of each stage (Y) of male of A. cucumeris could be fitted to the linear equation as follows: Temperature also influenced the survival of all immature stages except for the eggs (Table. 2). 2003 ZHANG ETAL: BIOLOGY OF AMBLWUSCUCUMERISFEEDING ON APONYCIIUSCORPUZAE 69
Population parameters of A. cucumeris feeding on A. corpuzae at 25a The net reproductive rate Ro per generation of A. cucumeris (20.80) was lower than it's prey A. corpuzae (21 54). The intrinsic rate of natural increase r,,, and finite rate of increase A ofa. cucumeris (0.175 and 1.191) were also lower than those of A. corpuzae (r,,, =0.185, A =1.202, Table 7, Fig. 2). TABLE 7. Parameters of population increase of A. cucumeris feeding on A. corpuzae at 25±1 Parameters A. cucumeris A. corpuzae Net reproductive rate Ro per generation 20.80 21.54 Intrinsic rate of natural increase r,,, day'* 0.175 0.185 Mean generation time T (days) 17.33 16.62 Finite rate of increase /I day"' 1.191 1.202 Age in days FIGURE 2. The Ix mx curve of A. cucumeris (dotted line) feeding on A. corpuzae and Ixmx curve of A. corpuzae (solid line) feeding on moso bamboo, all at 2S temperature condition. lx= agespeciffic mortality rate; ffix=(age-specific oviposition) x (proportion of females) x (egg hatchability). Discussion Our study at the individual level showed that A. cucumeris could develop, survive and increase its population when feeding on A. corpuzae. Our study of the population interactions also showed that at the initial predator-prey ratios between 3 : 30 and 9 : 30, A. cucumeris were capable of quickly bringing A. corpuzae under control, and the prey densities began to decrease from the 4th day after the predator introduction. These laboratory studies clearly suggest that A. cucumeris has good potential as a biological control agent of A. corpuzae. Since 1998, we have repeatedly released A. cucumeris into the moso bamboo forests to control A. corpuzae and other pest mites, and the pest occurrence has been reduced. The results of our study are especially interesting and encouraging because of (1) the lack of effective natural predators of A. corpuzae in bamboo forests and (2) the ease with which A. 72 SYSTEMATIC & APPLIED ACAROLOGY VOL. 8
cucumeris can be mass-produced for releases. T. hamhusae is the most abundant predatory mite in bamboo forests in Fujian. However, its density is rather low during the bamboo growing season. Our previous observations showed that T. hamhusae selectively feeds on A. corpuzae eggs but does not like to prey on its adults and irnrnatures. It was also reported in Japan that A. corpuzae is only a subsidiary or alternative prey for T. bambusae (Saito 1990). Another native predatory mite, Amhlysieus longispinosus Evans, also showed promise as a predator of A. corpuzae (Zhang et at. 1998), but it is not as easy to produce on a large scale as A. cucumeris. Therefore, it is necessary to investigate augmentative biological control using species such as A. cucumeris. In a previous study, we also showed that A. cucumeris can feed and develop well on Schizotetrancyhus nanjinegensis (Ma & Yuan), another important pest of moso bamboo in Fujian (Zhang et al. 1997,2000b). The impact ofa. cucumeris ona. corpusae will be greater thanits impact on S. nanjingensi.~ because A. corpuzae lacks the protection provided by the webnests in S, nanjinensis. A. cucumeris is therefore a valuable addition to the biocontrol weaponry against A. corpuzae on bamboo plants in Fujian. Acknowledgments This research was supported by the Office of International Co-operation, Science and Technology Commission of Fujian Province, China (99-1-2), the State Administration of Foreign Expert Affairs, Beijing, China, the Nippon Life Insurance Foundation, and Grants-in Aid of Scientific Research (B) (2) number 1357021 of JSPS. We thank Dr Qinghai Fan and Rosa Henderson (Landcare Research, Auckland) for reviews of the manuscript. References Bolland, H.R., Gutierrez, J. & Flechtmann, C.H.W. (1998) World Catalogue of the Spider Mite Family (Acari: Tetranychidae). Brill, Leiden, 392 pp. Brodeur, J., Bouchard, A. & Toucotte, G (1997) Potential of four species of predatory mites as biological control agents of the tomato russet mite, Aculops lycopersici (Massee) (Eriophyidae). The Canadian Entomologist, 129, 1-6. Croft, B.A., Pratt, P.D., Koskela, G. & Kaufinan, D. (1998) Predation, reproduction, and impact of phytoseiid mites (Acari: Phytoseiidae) on cyclamen mite (Acari: Tarsonemidae) on strawberry. Journal ofeconomic Entomology, 91(6), 1307-13 14. Gerson, U., Smiley, R.L & Ochoa, R. (2003) Mite's (Acari) for Pest Control. Blackwell Science Ltd., Oxford, UK, 539 pp. Saito, Y. (1990) Life history and food habit of Typhiodromus hamhusae Ehara, a specific predator of Schizotetranychus celarius (Banks) (Acari: Phytoseiidae, Tetranychidae). Experimental & Applied Acamlogy, 10, 45-51. Yu, H.-X. & Shi, J.-M. (1991) Studies on Schizotetranychus nanjingen.iis. Journal ofbamboo Research, 10(2), 61-67. [in Chinese with English abstract]. Tuovinen, T. (2000) Integrated control of the strawberry mite (Phytonemus pallidus) in the Nordic multi-year growing system. Acta Horticulturae, 525, 389-391. Tuovinen, T. (2002) Biological control of strawberry mite: a case study. Ada Hwticulturae, 567(2), 671-674. Zhang, Y. -X., Liu, Q.-Y., Lin, J.-Z., Song, M.-G., Cai, Q.-J. & He, X.-Y. (1997) Studies on species distribution and damage by spider mites in bamboo trees in Fujian province. Journal of Fujian Academy ofagricultural Sciences, 12(3), 11-15 [in Chinese with English abstract]. Zhang, Y.-X., Zhang, Z.-Q., Lin, J.-Z. & Liu, Q.-Y. (1998) Predation of Amhiy.veiuv longispinosus (Acari: Phytoseiidae) on Aponychus corpuzae (Acari: Tetranychidae). Systematic & Applied Acamlogy, 3,53-58. 2003 ZHANG ETAL: BIOLOGY OF AMBLY.YE1U.Y CUCUMERISFEEDING ON APONYCI1U.Y CORPUZAE 73
Zhaig, Y.-X., Zhang, Z.-Q., tin, J.-Z. & Ji, J. (2000a) Potential of Ambfy.~eiu.t cucumeris (Acari: Phytoseiidae) as a biocontrol agent against Schizotetranychus nanjingentis (Ace Tetranychidae) in Fujiau, China. Systematic & Applied Acarology Special Publications, 4, 109-1 24. Zhang, Y.-X., Zhang, Z.-Q. & Lin, J.Z., Song, M.-G & Ji, J. (2000b) Key factors affecting populations of Schizotetronychus nanjingensis. Aponychus corpuzae and Aculu.~ hamhu.vae in Fujian bamboo forests during different seasons: an analysis'using methods of grey sequence. Systematic & Applied. Acamlogy Special Publications. 4,125-1 60. Accepted30 June 2003 SYSTEMATIC & APPLIED ACAROLOGY VOL. 11