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Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae)
Biological Control 32 (2005) 378–384 www.elsevier.com/locate/ybcon
Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae) L.A. Escudero1, F. Ferragut* Instituto Agroforestal Mediterra´neo, Departamento de Ecosistemas Agroforestales, Universidad Polite´cnica, Camino de Vera, 14, 46022 Valencia, Spain Received 11 May 2004; accepted 23 December 2004
Abstract The commercially available strains of Phytoseiulus persimilis Athias-Henriot, the biological control agent of Tetranychus urticae Koch, perform poorly in the Western Mediterranean, probably because they are not well adapted to local climatic conditions. For that reason, efforts are being focused on the development of a biological control programme using native phytoseiid mites. Four species of red spider mites can be found in vegetable crops in eastern Spain: T. urticae, Tetranychus turkestani Ugarov and Nikolski, Tetranychus ludeni Zacher and the recently introduced Tetranychus evansi Baker and Pritchard. To evaluate their potential role as biological control agents, the present study evaluates the life-history of local populations of Neoseiulus californicus (McGregor) and P. persimilis when fed on T. urticae, T. turkestani, T. evansi, and T. ludeni in the laboratory. Results indicate that N. californicus and P. persimilis are able to feed and complete their development on the four tested red spider mite species. The predators may exhibit a particularly high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni, thus may be able to provide effective control of these species in the field. When fed T. evansi, however, predator performance was poor; significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity were recorded. The resultant low capacity for population growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. It is unlikely therefore that P. persimilis and N. californicus, now being widely used to control T. urticae in greenhouse crops in Central Europe, will be able to halt any spread of T. evansi to greenhouse crops in temperate areas. 2005 Elsevier Inc. All rights reserved. Keywords: Neoseiulus californicus; Phytoseiulus persimilis; Tetranychus evansi; Biological control; Life-history; Demographic parameters; Invasive species
1. Introduction Four species of red spider mites (Acari: Tetranychidae) maintain high population levels throughout the year in vegetable crops on the Spanish Mediterranean *
Corresponding author. Fax: +34 96 3879269. E-mail addresses: [email protected] (L.A. Escudero), [email protected] (F. Ferragut). 1 Present address: IRTA—Fundacio´ Mas Badia, La Tallada dÕEmporda`, 17134 Girona, Spain. 1049-9644/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2004.12.010
coast. These mites, namely Tetranychus urticae Koch, Tetranychus turkestani Ugarov and Nikolski, Tetranychus evansi Baker and Pritchard and Tetranychus ludeni Zacher, cause considerable damage to bean, melon, water melon, aubergine, tomato, strawberry, and pepper plants and many other outdoor and greenhouse crops. The two-spotted spider mite T. urticae and the strawberry spider mite T. turkestani are common whereas T. evansi and T. ludeni are abundant locally and can be found more often in warm coastal regions (Escudero, 1998; Escudero and Ferragut, 1998, 1999). A rich and
L.A. Escudero, F. Ferragut / Biological Control 32 (2005) 378–384
diverse fauna of phytoseiid predatory mites (Acari: Phytoseiidae) can also be found on these crops, of which, Neoseiulus californicus (McGregor) and Phytoseiulus persimilis Athias-Henriot are the most important species. N. californicus is the predominant predatory mite both on the crops and on the nearby unmanaged vegetation. This species shows tolerance to some pesticides and spontaneously colonizes the crops where it may suppress two-spotted spider mite populations (Escudero, 1998; Escudero and Ferragut, 1998, 1999). Traditionally, red spider mites have been controlled with acaricides, with the resulting problems of pest resistance and residue on the harvested and then consummed products. Biological control has not been widely adopted yet, probably because of its inconsistent results. P. persimilis has been an efficient biological control agent of the two-spotted spider mite T. urticae on indoor crops in Europe and North America since the late 60s (Lenteren and van Woets, 1988; Lenteren et al., 1992) and on outdoor crops in California and Florida (McMurtry, 1991). However, the commercially available strains of P. persimilis perform poorly in eastern Spain, probably because they are not well adapted to Mediterranean climatic conditions (Bakker et al., 1993; Nihoul, 1992; Stenseth, 1979). Efforts are therefore being devoted to the development of an integrated control programme of red spider mite species using native populations of phytoseiid mites. The four pestiferous red spider mite species are distributed over a large area where they may inhabit the same crops or even the same plants. For example, T. urticae and T. turkestani are often collected together on strawberry, melon, watermelon, and courgette, and at least in one ocasion T. urticae, T. turkestani, and T. ludeni have been observed on leaves of the same cucumber plant (Escudero, 1998). For this reason, biological control should deploy predators that can feed and reproduce on all four pest species. There is abundant information on the suitability of spider mites as a food source for N. californicus and P. persimilis. Yet most studies have used the two-spotted spider mite T. urticae (for a review see Helle and Sabelis, 1985), the Kanzawa spider mite Tetranychus kanzawai Kishida (Ashihara et al., 1978; Hamamura et al., 1976), the Pacific spider mite Tetranychus pacificus (Amano and Chant, 1977; Takahashi and Chant, 1994), the tomato spider mite T. evansi (Moraes and McMurtry, 1985) or the gorse spider mite Tetranychus lintearius (Dufour) (Pratt et al., 2003) as prey. Little is known about the influence of other prey species of the genus Tetranychus on the biology of phytoseiid predators. As the first step toward the utilization of phytoseiid predators in biological control of pestiferous mites, we evaluated here the life-history of native populations of N. californicus and P. persimilis when fed T. urticae, T. turkestani, T. evansi and T. ludeni in the laboratory.
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Then, we used the obtained demographic parameters to assess the potential of these predatory mites to suppress populations of these pests.
2. Materials and methods 2.1. Mite cultures Laboratory cultures of the mites were established from field collections of spider mite and phytoseiid species made in agricultural crops and weeds near Valencia (Spain). T. urticae and P. persimilis were collected on Phaseolus vulgaris L., T. turkestani, and N. californicus on Fragaria ananassa Duchesne, T. evansi on Solanum tuberosum L. and T. ludeni on Centaurea seridis L. (Compositae). Mite cultures were maintained in separate climatic rooms at 25 ± 1 C, 60–70% rh under a 16:8 h L:D. Spider mites were reared on bean plants, except T. evansi, which were produced on potato plants, a more suitable host. Predatory mites were reared on detached bean leaves prepared as follows. Several young, fully expanded bean leaves were placed underside up on a wet cotton wool layer in a plastic tray (35 · 20 cm). The wet cotton wool prevented mite escape and maintain leaf freshness for two weeks. The cotton wool was maintained wet by adding water where necessary. Bean leaves prepared as described above were infested with spider mites and 24 h later phytoseiid females of each species were transferred onto the leaves. Predatory mites were fed with mixed prey stages of T. urticae three times per week before the studies and with all the developmental stages of the tested prey for at least 20 days before performing the feeding trials (about three generations). 2.2. Predator feeding experiments Experiments were carried out in a climatic cabinet at 25 ± 1 C, 70–80% r.h. and under a 12:12 h L:D photoperiod. Twenty-five recently mated females of N. californicus and P. persimilis were confined in groups with sufficient prey to oviposit. Eggs were collected 24 h later, isolated in modified Huffaker cells (Overmeer, 1985; Sabelis, 1981), reared to the adult stage and observed until they died. These closed cells were prepared with a piece of plexiglas (8 · 4 cm and 5 mm of thickness) with a circular hole of diameter 2 cm in the middle of the plate. A second plexiglas plate of the same size forms the base of the cell. On this second plate, a moistened filter paper was laid on which a bean leaf was placed upside down. The piece of plexiglas with the hole was then placed on the leaf. A transparent coverslip closed the cell and all the pieces were held together with rubber bands. This method is mite proof and allowed easy observation of the mites under a dissecting microscope.
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Predatory mites were reared with ample of prey that was replenished daily. Bean leaves were replaced every 3–4 days and phytoseiid mites were transferred to new isolation cells with a camelÕs hair brush. During the juvenile stages, leaf discs were checked every 8 h and the presence of exuvia was used as evidence moulting. A male was added to each cell after the last moult. Survival and the number of deposited eggs was recorded daily until all females had died. Each test was consisted of 45–65 individually reared mites. 2.3. Statistical analyses Data on developmental time, duration of female reproductive periods and fecundity were analyzed using one-way ANOVA followed by the LSD test to compare data means (SPSS, 1999). Daily age-specific survival (lx) and fecundity rates (mx) were used to generate life-tables for each phytoseiid species and food combination. The intrinsic rates of increase (rm) were estimated by non linear regression using the equation (Birch, P1Lotka–Euler rx 1948; Lotka, 1924): lx mx ¼ 1, where r is the 0 e intrinsic rate of natural increase (rm), x is female age, lx is the fraction of females surviving to age x and mx is the expected number of daughters produced per female alive at age x, obtained by multiplying the number of eggs by the sex ratio. Differences in rm values between treatment combinations were tested using the Jacknife method proposed by Hulting et al. (1990). This program is based on the BirchÕs method and Jacknife procedures that uses the variance and standard error of each calculated parameter. The Student–Newman–Keuls test was used to evaluate differences between rm values.
3. Results 3.1. Effects of prey on predator development and sex-ratio The two predator species successfully completed their development feeding on the four prey species (Table 1).
Their survival to adulthood, however, differed among diets. Between 91 and 98% of the predators fed T. urticae, T. turkestani, and T. ludeni reached reproductive maturity whereas only between 68 and 76% of N. californicus and P. persimilis reached that stage when fed on T. evansi. Predator development time was likewise affected by the food prey; egg to adult was significantly longer when N. californicus and P. persimilis (F = 30.20; df = 3, 8; P < 0.0001 and F = 88.84; df = 3, 8; P < 0.0001, respectively) were fed T. evansi than the other prey species. The sex ratio of the two phytoseiid species was less female biased when the prey was T. evansi. The proportion of females to males offspring when N. californicus and P. persimilis fed on T. urticae, T. turkestani, and T. ludeni was about of two to one, whereas only a half of females were produced on T. evansi diet. 3.2. Influence prey on age-specific survival and birth rate The age-specific survival lx (percentage of surviving females at the instant x) and age-specific fecundity rate mx (number of female eggs laid per female per day) for N. californicus and P. persimilis fed on four Tetranychus species are shown in Figs. 1 and 2. N. californicus and P. persimilis show similar survival curves when fed on T. urticae, T. turkestani, and T. ludeni. Both species exhibited high survival levels during the first 15–20 days of the trial, and their survival subsequently decreased rapidly. When fed T. evansi, however, survival rate started to decrease after the first few days. In all the cases, the form of the time-specific fecundity curve was triangular or trapezoid. Oviposition rate increased rapidly from the beginning of the reproductive period to its peak; it then roughly leveled off. Oviposition rate subsequently decreased gradually until the end of the reproductive stage. Oviposition rate peaked during the first two to five days of oviposition phase for P. persimilis and between days five and seven in N. californicus. Oviposition curves were always smaller when the phytoseiids were fed T. evansi than the other prey species. As a result, oviposition period was shorter
Table 1 Development time in hours (mean ± 1SD), survival of immature stages and sex-ratio of N. californicus and P. persimilis when fed four spider mite species Egg
Larva
Protonymph
Deutonymph
Egg to adult
Survival to adulthood (%)
Sex-ratio
Neoseiulus californicus T. urticae 57.78 ± 8.96 T. turkestani 50.30 ± 5.40 T. ludeni 44.44 ± 5.04 T. evansi 54.60 ± 3.79
a a a a
22.34 ± 5.15 25.85 ± 4.40 21.18 ± 3.64 24.74 ± 3.25
a a a a
40.44 ± 6.58 36.45 ± 6.54 26.12 ± 4.99 58.14 ± 3.94
b b b a
34.43 ± 6.76 30.46 ± 3.65 20.41 ± 4.69 45.33 ± 4.50
b b c a
154.98 ± 11.32 b 143.06 ± 11.53 b 112.15 ± 5.26 c 182.81 ± 7.18 a
93.2 91.4 97.1 75.7
73.98 68.21 74.75 55.79
Phytoseiulus persimilis T. urticae 34.83 ± 2.89 T. turkestani 44.09 ± 4.51 T. ludeni 34.40 ± 3.24 T. evansi 43.93 ± 5.12
a a a a
15.83 ± 5.06 13.11 ± 3.61 13.93 ± 1.72 19.18 ± 5.65
a a a a
24.11 ± 3.06 35.77 ± 4.07 26.20 ± 2.88 47.04 ± 3.70
c b c a
25.06 ± 4.85 21.11 ± 3.07 17.13 ± 3.15 55.71 ± 5.05
b bc c a
99.83 ± 7.20 114.61 ± 4.20 91.66 ± 6.08 165.86 ± 6.58
96.2 94.9 98.1 67.8
73.89 72.17 77.65 50.20
c b c a
Sex-ratio (percent of females). Numbers within the same column followed by different letters are significantly different (LSD Test, P < 0.05).
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Fig. 1. Age-specific survivorship (lx) and age-specific birth rate (mx) of N. californicus fed on four species of Tetranychus.
and oviposition rate was lower when the predators were fed T. evansi. Peak oviposition rate was between 3.05 and 3.99 eggs per day per N. californicus female when fed T. urticae, T. turkestani, and T. ludeni. Oviposition rate only reached the value of 0.90 eggs per female per day when fed on T. evansi. 3.3. Effects of prey on reproductive and life table parameters Prey also influenced the duration of the preoviposition and oviposition periods (Table 2). Time to first egg deposition was between 2.5 and 3.2 times longer when N. californicus was fed T. evansi (F = 48.89, df = 3, 8, P < 0.0001) and 3.3 times longer when P. persimilis was fed T. evansi (F = 73.40, df = 3, 8, P < 0.0001) compared to their preoviposition time when fed on the other spider mite species. In contrast, the time required for oviposition was considerably shorter when N. californicus (F = 6.73, df = 3, 8, P = 0.0140) and P. persimilis (F = 8.01, df = 3, 8, P = 0.0085) fed on T. evansi. The obtained values represent a reduction in the oviposition period of 78–79 and 57–61%, respectively for the two predators when compared to the other prey diets. In addition, when females of the two phytoseiids feed on T. evansi they produced fewer eggs towards the end
of their lives and at a slower rate than when they feed on the other prey. Data show that life-time fecundity and oviposition rate were significantly lower when N. californicus (F = 302.60, df = 3, 8, P < 0.0001; F = 2.29, df = 3, 8, P = 0.1154) and P. persimilis (F = 571.23, df = 3, 8, P < 0.0001; F = 13.77, df = 3, 8, P = 0.0016) were fed T. evansi compared to other prey species. The life-time fecundity was about 6 eggs/female for N. californicus, 90% less than that obtained with other prey, and 9 eggs/female for P. persimilis, which represents 86% fewer eggs than when they feed on T. urticae or T. ludeni. This predator lays fewer eggs on T. turkestani than on T. urticae or T. ludeni. When fed on T. evansi, females of N. californicus and P. persimilis were only able to produce about one egg by female and day, between three and four times less than that produced with other prey species. rm values did not differ significantly for N. californicus (F = 388.02, df = 3, 8, P < 0.0001) and P. persimilis (F = 3609.22, df = 3, 8, P < 0.0001) when fed T. urticae, T. turkestani, and T. ludeni. Much lower values were obtained, however, when fed T. evansi. In both predatory mites this was due to the small production of offspring, with the net reproduction values R0 of 3.33 females/generation for N. californicus and 4.37 females/generation for P. persimilis, rather than to differences in the gener-
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Fig. 2. Age-specific survivorship (lx) and age-specific birth rate (mx) of P. persimilis fed on four species of Tetranychus.
ation time T. These data represent a reduction of 92% for N. californicus and 90% for P. persimilis in their net reproduction while feeding on T. evansi.
4. Discussion Results demonstrate that local populations of N. californicus and P. persimilis are able to feed and complete
their development on the four tested red spider mite species. The predators may exhibit a high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni thus may be able to provide effective control of these mite species in the field. When fed T. evansi, however, predatorsÕ performance was poor. We recorded a significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity. The resultant low capacity for population
Table 2 Effect of four species of spider mite prey on duration of female reproductive periods and life table parameters of N. californicus and P. persimilis Preoviposition (h)*
Oviposition period (d)*
Total fecundity*
Oviposition rate*
R0
T
rm**
Neoseiulus californicus T. urticae 28.65 ± 1.73 b T. turkestani 30.00 ± 2.69 b T. ludeni 24.00 ± 2.33 b T. evansi 76.38 ± 11.50 a
20.48 ± 5.97 20.35 ± 6.12 21.15 ± 5.30 4.32 ± 2.89
a a a b
56.67 ± 2.80 58.64 ± 2.69 63.11 ± 3.11 5.95 ± 1.61
a a a b
2.70 ± 1.13 2.66 ± 1.06 2.97 ± 0.45 0.79 ± 0.90
a a a b
49.25 42.93 47.37 3.33
17.46 17.89 16.04 14.50
0.283 0.267 0.337 0.084
a a a b
Phytoseiulus persimilis T. urticae 27.84 ± 2.16 b T. turkestani 26.4 ± 1.344 b T. ludeni 24.09 ± 4.30 b T. evansi 79.29 ± 9.54 a
16.09 ± 1.84 a 15.78 ± 2.31a 14.69 ± 4.07 a 6.33 ± 2.62 b
61.71 ± 2.17 57.90 ± 1.69 63.98 ± 2.10 8.77 ± 1.61
a b a c
3.97 ± 0.37 3.84 ± 0.35 3.79 ± 0.41 1.17 ± 0.76
a a a b
45.61 43.02 40.78 4.37
12.85 12.79 11.57 14.21
0.373 0.367 0.424 0.106
a a a b
Total fecundity (eggs/female); oviposition rate (eggs/female/day); R0 (net reproductive rate in females/female); T (mean generation time in days); rm (intrinsic rate of increase in days1). Numbers within the same column followed by different letters are significantly different. * LSD test, P < 0.05. ** Student–Newman–Keuls test, P = 0.05.
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growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. The inability of phytoseiids to develop adequately when feeding on T. evansi has already been demonstrated for Euseius concordis (Chant) by Moraes and Lima (1983), for eight predatory mite species, including P. persimilis and N. californicus, by Moraes and McMurtry (1985), and more recently by Sarr et al. (2002) against this spider mite in Kenya. These studies revealed that none of the tested phytoseiid species were effective predators of the tomato spider mite. In all cases the oviposition and survival rates of predatory mites were low on this prey. Tetranychus evansi is an invasive species recently introduced into Spain, where it was first found on potato plants at the end of 1995 (Ferragut and Escudero, 1999). Since then, it has rapidly spread throughout the Spanish Mediterranean coast and the Canary Islands, causing considerable damage to tomato, aubergine, and potato plants, both outdoors and in greenhouses. Recent attempts to control the pest through mass releases of predatory mites, mainly P. persimilis, on tomatoes in some locations of the Mediterranean coast and the Canary Islands, have been unsuccessful. Plants may affect predatory mites through modifications of the suitability of its prey. Solanaceous plants produce secondary plant chemicals, like methil-ketones, and sesquiterpenes highly toxic for mites and insects (Chatzivasileiadis and Sabelis, 1997; Maluf et al., 2001). Poor efficacy of the predators in the present study may be due, at least in part, to the secondary plant compounds consumed while T. evansi was reared on potatoes. These possible effects may have caused a delay in protonymphal and deutonymphal development in both predatory mites. Furthermore, acquisition of secondary compounds by T. evansi may have affected predator reproduction through their act as feeding depressants as suggested by Moraes and McMurtry (1987) for P. persimilis and T. urticae reared on Solanum douglasi Dunal. Additional studies are needed to establish the reasons of the inefficiency of predatory mites on T. evansi and to determine whether phytoseiids are able to control the prey reared on other host than solanaceous plants. Tetranychus evansi continues to spread northwards up the Mediterranean coast and may already be found near the French border. In the absence of effective biological control agents, this species may soon threaten greenhouse crops in Central Europe. Its invasion of temperate protected crops may disrupt the ongoing efficient biological control program against T. urticae through mass releases of P. persimilis and N. californicus.
Acknowledgments The authors thank two anonymous referees for their useful comments on the first version of the manuscript.
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We are also grateful to Dr. Lourival Costa Paraı´ba from EMBRAPA, Meio Ambiente, Jaguariu´na, Sao Paulo (Brazil) for his assistance in life table data analysis. This research was funded by the Comisio´n Interministerial de Ciencia y Tecnologı´a (CICYT), Project AGF95-0826, and the Ministerio de Ciencia y Tecnologı´a (MCYT), Project AGL2003-05041.
References Amano, H., Chant, D.A., 1977. Life history and reproduction of two species of predacious mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni (Chant) (Acarina: Phytoseiidae). Canadian J. Zool. 55, 1978–1983. Ashihara, W., Hamamura, T., Shinkaji, N., 1978. Feeding, reproduction and development of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae) on various food substances. Bull. Fruit Tree Res. Stn. Japan E2, 91–98. Bakker, F.M., Klein, M.E., Mesa, N.C., Braun, A.R., 1993. Saturation deficit tolerance spectra of phytophagous mites and their phytoseiid predators on cassava. Exp. Appl. Acarol. 17, 97–113. Birch, L.C., 1948. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol. 17, 15–26. Chatzivasileiadis, E.A., Sabelis, M.W., 1997. Toxicity of methyl ketones from tomato trichomes to Tetranychus urticae. Exp. Appl. Acarol. 21, 473–484. Escudero, L.A., 1998. Estructura y dina´mica de las comunidades de a´caros del ecosistema hortı´cola mediterra´neo: bases para el empleo de fitoseidos en el control biolo´gico de las aran˜as rojas. Ph.D. Thesis. Universidad Polite´cnica de Valencia. (In Spanish). Escudero, L.A., Ferragut, F., 1998. Comunidades de a´caros del ecosistema hortı´cola mediterra´neo: composicio´n y distribucio´n geogra´fica. Bol. San. Veg., Plagas. 24, 749–762 (In Spanish). Escudero, L.A., Ferragut, F., 1999. Abundancia y dina´mica estacional de las poblaciones de fitoseidos en los cultivos hortı´colas valencianos (Acari: Tetranychidae, Phytoseiidae). Bol. San. Veg., Plagas. 25, 347–362 (In Spanish). Ferragut, F., Escudero, L.A., 1999. Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), una nueva aran˜a roja en los cultivos hortı´colas espan˜oles. Bol. San. Veg., Plagas. 25, 157–164 (In Spanish). Hamamura, T., Shinkaji, N., Ashihara, W., 1976. The relationship between temperature and developmental period, and oviposition of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae). Bull. Fruit Tree Res. Stn., Japan E1, 117–125. Helle, W., Sabelis, M.W. (Eds.), 1985. Spider Mites: Their Biology, Natural Enemies and Control, vol. 1B. World Crop Pests. Elsevier. Hulting, F.L., Orr, D.B., Obrycki, J.J., 1990. A computer program for calculation and statistical comparison of intrinsic rates of increase and associated life table parameters. Florida Entomol. 73, 601–612. Lenteren, J.C., van Woets, J., 1988. Biological and integrated pest control in greenhouses. Annu. Rev. Entomol. 33, 239–269. Lenteren, J.C., van Benuzzi, M., Nicoli, G., Maini, S., 1992. Biological control in protected crops in Europe. In: van Lenteren, J.C., Minks, A.K., de Ponti, O.M.B. (Eds.), In Biological Control and Integrated Crop Protection: Towards Environmentally Safer Agriculture. Pudoc Scientific Publishers, Wageningen, pp. 77–98. Lotka, A.J., 1924. Elements of Physical Biology. Williams & Wilkins, Baltimore, p. 460. Maluf, W.R., Canpos, G.A., Cardose, M.G., 2001. Relationships between trichome types and spider mite (Tetranychus evansi) repellence in tomatoes with respect to foliar zingiberene contents. Euphytica 121, 73–80.
384
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McMurtry, J.A., 1991. Augmentative releases to control mites in agriculture. In: Dusbabek, F., Bukva, V. (Eds.), Modern Acarology, vol. 1. SPB Academic Publ., Prague, pp. 151–157, p. 651. Moraes, G.J., Lima, H.C., 1983. Biology of Euseius concordis (Chant) (Acarina: Phytoseiidae) a predator of the tomato russet mite. Acarologia 24, 251–255. Moraes, G.J., McMurtry, J.A., 1985. Comparison of Tetranychus evansi and T. urticae (Acari: Tetranychidae) as prey for eight species of phytoseiid mites. Entomophaga 30 (4), 393–397. Moraes, G.J., McMurtry, J.A., 1987. Physiological effect of the host plant on the suitability of Tetranychus urticae as prey for Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae). Entomophaga 32 (1), 35–38. Nihoul, P., 1992. Effect of temperature and relative humidity on successful control of Tetranychus urticae Koch by Phytoseiulus persimilis Athias-Henriot (Acari; Tetranychidae, Phytoseiidae) in tomato crops under glasshouse conditions. Med. Fac. Landbouww. Rijksuniv Gent. 57, 949–957. Overmeer, W.P.J., 1985. Rearing and handling. In: Helle, W., Sabelis, M.W. (Eds.), Spider Mites: Their biology, natural enemies and control. World Crop Pests. Elsevier.
Pratt, P.D., Coombs, E.M., Croft, B.A., 2003. Predation by phytoseiid mites on Tetranychus lintearius (Acari: Tetranychidae), an established weed biological control agent of gorse (Ulex europaeus). Biol. Control 26, 40–47. Sabelis, M.W., 1981. Biological control of two-spotted spider mites using phytoseiid predators. Part I: modelling the predator-prey interaction at the individual level. Agricultural Research Reports, Pudoc, Wageningen, p. 242. Sarr, I., Knapp, M., Ogol, C.K.P., Baumga¨rtner, J., 2002. Impact of predators on Tetranychus evansi Baker and Pritchard populations and damage on tomatoes (Lycopersicon esculentum Mill.) in Kenya. XI Int. Congress Acarology, Merida, Mexico. Abstract Book: 271. SPSS, 1999. SPSS Base 10.0 Application Guide. SPSS. Chicago. Stenseth, C., 1979. The effect of temperature and humidity on the development of Phytoseiulus persimilis and its ability to regulate populations of Tetranychus urticae (Acarina: Tetranychidae, Phytoseiidae). Entomophaga 24, 311–317. Takahashi, F., Chant, D.A., 1994. Adaptative strategies in the genus Phytoseiulus Evans (Acari: Phytoseiidae). II. Survivorship and reproduction. Int. J. Acarol. 20 (2), 87–96.
Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae) L.A. Escudero1, F. Ferragut* Instituto Agroforestal Mediterra´neo, Departamento de Ecosistemas Agroforestales, Universidad Polite´cnica, Camino de Vera, 14, 46022 Valencia, Spain Received 11 May 2004; accepted 23 December 2004
Abstract The commercially available strains of Phytoseiulus persimilis Athias-Henriot, the biological control agent of Tetranychus urticae Koch, perform poorly in the Western Mediterranean, probably because they are not well adapted to local climatic conditions. For that reason, efforts are being focused on the development of a biological control programme using native phytoseiid mites. Four species of red spider mites can be found in vegetable crops in eastern Spain: T. urticae, Tetranychus turkestani Ugarov and Nikolski, Tetranychus ludeni Zacher and the recently introduced Tetranychus evansi Baker and Pritchard. To evaluate their potential role as biological control agents, the present study evaluates the life-history of local populations of Neoseiulus californicus (McGregor) and P. persimilis when fed on T. urticae, T. turkestani, T. evansi, and T. ludeni in the laboratory. Results indicate that N. californicus and P. persimilis are able to feed and complete their development on the four tested red spider mite species. The predators may exhibit a particularly high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni, thus may be able to provide effective control of these species in the field. When fed T. evansi, however, predator performance was poor; significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity were recorded. The resultant low capacity for population growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. It is unlikely therefore that P. persimilis and N. californicus, now being widely used to control T. urticae in greenhouse crops in Central Europe, will be able to halt any spread of T. evansi to greenhouse crops in temperate areas. 2005 Elsevier Inc. All rights reserved. Keywords: Neoseiulus californicus; Phytoseiulus persimilis; Tetranychus evansi; Biological control; Life-history; Demographic parameters; Invasive species
1. Introduction Four species of red spider mites (Acari: Tetranychidae) maintain high population levels throughout the year in vegetable crops on the Spanish Mediterranean *
Corresponding author. Fax: +34 96 3879269. E-mail addresses: [email protected] (L.A. Escudero), [email protected] (F. Ferragut). 1 Present address: IRTA—Fundacio´ Mas Badia, La Tallada dÕEmporda`, 17134 Girona, Spain. 1049-9644/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2004.12.010
coast. These mites, namely Tetranychus urticae Koch, Tetranychus turkestani Ugarov and Nikolski, Tetranychus evansi Baker and Pritchard and Tetranychus ludeni Zacher, cause considerable damage to bean, melon, water melon, aubergine, tomato, strawberry, and pepper plants and many other outdoor and greenhouse crops. The two-spotted spider mite T. urticae and the strawberry spider mite T. turkestani are common whereas T. evansi and T. ludeni are abundant locally and can be found more often in warm coastal regions (Escudero, 1998; Escudero and Ferragut, 1998, 1999). A rich and
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diverse fauna of phytoseiid predatory mites (Acari: Phytoseiidae) can also be found on these crops, of which, Neoseiulus californicus (McGregor) and Phytoseiulus persimilis Athias-Henriot are the most important species. N. californicus is the predominant predatory mite both on the crops and on the nearby unmanaged vegetation. This species shows tolerance to some pesticides and spontaneously colonizes the crops where it may suppress two-spotted spider mite populations (Escudero, 1998; Escudero and Ferragut, 1998, 1999). Traditionally, red spider mites have been controlled with acaricides, with the resulting problems of pest resistance and residue on the harvested and then consummed products. Biological control has not been widely adopted yet, probably because of its inconsistent results. P. persimilis has been an efficient biological control agent of the two-spotted spider mite T. urticae on indoor crops in Europe and North America since the late 60s (Lenteren and van Woets, 1988; Lenteren et al., 1992) and on outdoor crops in California and Florida (McMurtry, 1991). However, the commercially available strains of P. persimilis perform poorly in eastern Spain, probably because they are not well adapted to Mediterranean climatic conditions (Bakker et al., 1993; Nihoul, 1992; Stenseth, 1979). Efforts are therefore being devoted to the development of an integrated control programme of red spider mite species using native populations of phytoseiid mites. The four pestiferous red spider mite species are distributed over a large area where they may inhabit the same crops or even the same plants. For example, T. urticae and T. turkestani are often collected together on strawberry, melon, watermelon, and courgette, and at least in one ocasion T. urticae, T. turkestani, and T. ludeni have been observed on leaves of the same cucumber plant (Escudero, 1998). For this reason, biological control should deploy predators that can feed and reproduce on all four pest species. There is abundant information on the suitability of spider mites as a food source for N. californicus and P. persimilis. Yet most studies have used the two-spotted spider mite T. urticae (for a review see Helle and Sabelis, 1985), the Kanzawa spider mite Tetranychus kanzawai Kishida (Ashihara et al., 1978; Hamamura et al., 1976), the Pacific spider mite Tetranychus pacificus (Amano and Chant, 1977; Takahashi and Chant, 1994), the tomato spider mite T. evansi (Moraes and McMurtry, 1985) or the gorse spider mite Tetranychus lintearius (Dufour) (Pratt et al., 2003) as prey. Little is known about the influence of other prey species of the genus Tetranychus on the biology of phytoseiid predators. As the first step toward the utilization of phytoseiid predators in biological control of pestiferous mites, we evaluated here the life-history of native populations of N. californicus and P. persimilis when fed T. urticae, T. turkestani, T. evansi and T. ludeni in the laboratory.
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Then, we used the obtained demographic parameters to assess the potential of these predatory mites to suppress populations of these pests.
2. Materials and methods 2.1. Mite cultures Laboratory cultures of the mites were established from field collections of spider mite and phytoseiid species made in agricultural crops and weeds near Valencia (Spain). T. urticae and P. persimilis were collected on Phaseolus vulgaris L., T. turkestani, and N. californicus on Fragaria ananassa Duchesne, T. evansi on Solanum tuberosum L. and T. ludeni on Centaurea seridis L. (Compositae). Mite cultures were maintained in separate climatic rooms at 25 ± 1 C, 60–70% rh under a 16:8 h L:D. Spider mites were reared on bean plants, except T. evansi, which were produced on potato plants, a more suitable host. Predatory mites were reared on detached bean leaves prepared as follows. Several young, fully expanded bean leaves were placed underside up on a wet cotton wool layer in a plastic tray (35 · 20 cm). The wet cotton wool prevented mite escape and maintain leaf freshness for two weeks. The cotton wool was maintained wet by adding water where necessary. Bean leaves prepared as described above were infested with spider mites and 24 h later phytoseiid females of each species were transferred onto the leaves. Predatory mites were fed with mixed prey stages of T. urticae three times per week before the studies and with all the developmental stages of the tested prey for at least 20 days before performing the feeding trials (about three generations). 2.2. Predator feeding experiments Experiments were carried out in a climatic cabinet at 25 ± 1 C, 70–80% r.h. and under a 12:12 h L:D photoperiod. Twenty-five recently mated females of N. californicus and P. persimilis were confined in groups with sufficient prey to oviposit. Eggs were collected 24 h later, isolated in modified Huffaker cells (Overmeer, 1985; Sabelis, 1981), reared to the adult stage and observed until they died. These closed cells were prepared with a piece of plexiglas (8 · 4 cm and 5 mm of thickness) with a circular hole of diameter 2 cm in the middle of the plate. A second plexiglas plate of the same size forms the base of the cell. On this second plate, a moistened filter paper was laid on which a bean leaf was placed upside down. The piece of plexiglas with the hole was then placed on the leaf. A transparent coverslip closed the cell and all the pieces were held together with rubber bands. This method is mite proof and allowed easy observation of the mites under a dissecting microscope.
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Predatory mites were reared with ample of prey that was replenished daily. Bean leaves were replaced every 3–4 days and phytoseiid mites were transferred to new isolation cells with a camelÕs hair brush. During the juvenile stages, leaf discs were checked every 8 h and the presence of exuvia was used as evidence moulting. A male was added to each cell after the last moult. Survival and the number of deposited eggs was recorded daily until all females had died. Each test was consisted of 45–65 individually reared mites. 2.3. Statistical analyses Data on developmental time, duration of female reproductive periods and fecundity were analyzed using one-way ANOVA followed by the LSD test to compare data means (SPSS, 1999). Daily age-specific survival (lx) and fecundity rates (mx) were used to generate life-tables for each phytoseiid species and food combination. The intrinsic rates of increase (rm) were estimated by non linear regression using the equation (Birch, P1Lotka–Euler rx 1948; Lotka, 1924): lx mx ¼ 1, where r is the 0 e intrinsic rate of natural increase (rm), x is female age, lx is the fraction of females surviving to age x and mx is the expected number of daughters produced per female alive at age x, obtained by multiplying the number of eggs by the sex ratio. Differences in rm values between treatment combinations were tested using the Jacknife method proposed by Hulting et al. (1990). This program is based on the BirchÕs method and Jacknife procedures that uses the variance and standard error of each calculated parameter. The Student–Newman–Keuls test was used to evaluate differences between rm values.
3. Results 3.1. Effects of prey on predator development and sex-ratio The two predator species successfully completed their development feeding on the four prey species (Table 1).
Their survival to adulthood, however, differed among diets. Between 91 and 98% of the predators fed T. urticae, T. turkestani, and T. ludeni reached reproductive maturity whereas only between 68 and 76% of N. californicus and P. persimilis reached that stage when fed on T. evansi. Predator development time was likewise affected by the food prey; egg to adult was significantly longer when N. californicus and P. persimilis (F = 30.20; df = 3, 8; P < 0.0001 and F = 88.84; df = 3, 8; P < 0.0001, respectively) were fed T. evansi than the other prey species. The sex ratio of the two phytoseiid species was less female biased when the prey was T. evansi. The proportion of females to males offspring when N. californicus and P. persimilis fed on T. urticae, T. turkestani, and T. ludeni was about of two to one, whereas only a half of females were produced on T. evansi diet. 3.2. Influence prey on age-specific survival and birth rate The age-specific survival lx (percentage of surviving females at the instant x) and age-specific fecundity rate mx (number of female eggs laid per female per day) for N. californicus and P. persimilis fed on four Tetranychus species are shown in Figs. 1 and 2. N. californicus and P. persimilis show similar survival curves when fed on T. urticae, T. turkestani, and T. ludeni. Both species exhibited high survival levels during the first 15–20 days of the trial, and their survival subsequently decreased rapidly. When fed T. evansi, however, survival rate started to decrease after the first few days. In all the cases, the form of the time-specific fecundity curve was triangular or trapezoid. Oviposition rate increased rapidly from the beginning of the reproductive period to its peak; it then roughly leveled off. Oviposition rate subsequently decreased gradually until the end of the reproductive stage. Oviposition rate peaked during the first two to five days of oviposition phase for P. persimilis and between days five and seven in N. californicus. Oviposition curves were always smaller when the phytoseiids were fed T. evansi than the other prey species. As a result, oviposition period was shorter
Table 1 Development time in hours (mean ± 1SD), survival of immature stages and sex-ratio of N. californicus and P. persimilis when fed four spider mite species Egg
Larva
Protonymph
Deutonymph
Egg to adult
Survival to adulthood (%)
Sex-ratio
Neoseiulus californicus T. urticae 57.78 ± 8.96 T. turkestani 50.30 ± 5.40 T. ludeni 44.44 ± 5.04 T. evansi 54.60 ± 3.79
a a a a
22.34 ± 5.15 25.85 ± 4.40 21.18 ± 3.64 24.74 ± 3.25
a a a a
40.44 ± 6.58 36.45 ± 6.54 26.12 ± 4.99 58.14 ± 3.94
b b b a
34.43 ± 6.76 30.46 ± 3.65 20.41 ± 4.69 45.33 ± 4.50
b b c a
154.98 ± 11.32 b 143.06 ± 11.53 b 112.15 ± 5.26 c 182.81 ± 7.18 a
93.2 91.4 97.1 75.7
73.98 68.21 74.75 55.79
Phytoseiulus persimilis T. urticae 34.83 ± 2.89 T. turkestani 44.09 ± 4.51 T. ludeni 34.40 ± 3.24 T. evansi 43.93 ± 5.12
a a a a
15.83 ± 5.06 13.11 ± 3.61 13.93 ± 1.72 19.18 ± 5.65
a a a a
24.11 ± 3.06 35.77 ± 4.07 26.20 ± 2.88 47.04 ± 3.70
c b c a
25.06 ± 4.85 21.11 ± 3.07 17.13 ± 3.15 55.71 ± 5.05
b bc c a
99.83 ± 7.20 114.61 ± 4.20 91.66 ± 6.08 165.86 ± 6.58
96.2 94.9 98.1 67.8
73.89 72.17 77.65 50.20
c b c a
Sex-ratio (percent of females). Numbers within the same column followed by different letters are significantly different (LSD Test, P < 0.05).
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Fig. 1. Age-specific survivorship (lx) and age-specific birth rate (mx) of N. californicus fed on four species of Tetranychus.
and oviposition rate was lower when the predators were fed T. evansi. Peak oviposition rate was between 3.05 and 3.99 eggs per day per N. californicus female when fed T. urticae, T. turkestani, and T. ludeni. Oviposition rate only reached the value of 0.90 eggs per female per day when fed on T. evansi. 3.3. Effects of prey on reproductive and life table parameters Prey also influenced the duration of the preoviposition and oviposition periods (Table 2). Time to first egg deposition was between 2.5 and 3.2 times longer when N. californicus was fed T. evansi (F = 48.89, df = 3, 8, P < 0.0001) and 3.3 times longer when P. persimilis was fed T. evansi (F = 73.40, df = 3, 8, P < 0.0001) compared to their preoviposition time when fed on the other spider mite species. In contrast, the time required for oviposition was considerably shorter when N. californicus (F = 6.73, df = 3, 8, P = 0.0140) and P. persimilis (F = 8.01, df = 3, 8, P = 0.0085) fed on T. evansi. The obtained values represent a reduction in the oviposition period of 78–79 and 57–61%, respectively for the two predators when compared to the other prey diets. In addition, when females of the two phytoseiids feed on T. evansi they produced fewer eggs towards the end
of their lives and at a slower rate than when they feed on the other prey. Data show that life-time fecundity and oviposition rate were significantly lower when N. californicus (F = 302.60, df = 3, 8, P < 0.0001; F = 2.29, df = 3, 8, P = 0.1154) and P. persimilis (F = 571.23, df = 3, 8, P < 0.0001; F = 13.77, df = 3, 8, P = 0.0016) were fed T. evansi compared to other prey species. The life-time fecundity was about 6 eggs/female for N. californicus, 90% less than that obtained with other prey, and 9 eggs/female for P. persimilis, which represents 86% fewer eggs than when they feed on T. urticae or T. ludeni. This predator lays fewer eggs on T. turkestani than on T. urticae or T. ludeni. When fed on T. evansi, females of N. californicus and P. persimilis were only able to produce about one egg by female and day, between three and four times less than that produced with other prey species. rm values did not differ significantly for N. californicus (F = 388.02, df = 3, 8, P < 0.0001) and P. persimilis (F = 3609.22, df = 3, 8, P < 0.0001) when fed T. urticae, T. turkestani, and T. ludeni. Much lower values were obtained, however, when fed T. evansi. In both predatory mites this was due to the small production of offspring, with the net reproduction values R0 of 3.33 females/generation for N. californicus and 4.37 females/generation for P. persimilis, rather than to differences in the gener-
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Fig. 2. Age-specific survivorship (lx) and age-specific birth rate (mx) of P. persimilis fed on four species of Tetranychus.
ation time T. These data represent a reduction of 92% for N. californicus and 90% for P. persimilis in their net reproduction while feeding on T. evansi.
4. Discussion Results demonstrate that local populations of N. californicus and P. persimilis are able to feed and complete
their development on the four tested red spider mite species. The predators may exhibit a high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni thus may be able to provide effective control of these mite species in the field. When fed T. evansi, however, predatorsÕ performance was poor. We recorded a significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity. The resultant low capacity for population
Table 2 Effect of four species of spider mite prey on duration of female reproductive periods and life table parameters of N. californicus and P. persimilis Preoviposition (h)*
Oviposition period (d)*
Total fecundity*
Oviposition rate*
R0
T
rm**
Neoseiulus californicus T. urticae 28.65 ± 1.73 b T. turkestani 30.00 ± 2.69 b T. ludeni 24.00 ± 2.33 b T. evansi 76.38 ± 11.50 a
20.48 ± 5.97 20.35 ± 6.12 21.15 ± 5.30 4.32 ± 2.89
a a a b
56.67 ± 2.80 58.64 ± 2.69 63.11 ± 3.11 5.95 ± 1.61
a a a b
2.70 ± 1.13 2.66 ± 1.06 2.97 ± 0.45 0.79 ± 0.90
a a a b
49.25 42.93 47.37 3.33
17.46 17.89 16.04 14.50
0.283 0.267 0.337 0.084
a a a b
Phytoseiulus persimilis T. urticae 27.84 ± 2.16 b T. turkestani 26.4 ± 1.344 b T. ludeni 24.09 ± 4.30 b T. evansi 79.29 ± 9.54 a
16.09 ± 1.84 a 15.78 ± 2.31a 14.69 ± 4.07 a 6.33 ± 2.62 b
61.71 ± 2.17 57.90 ± 1.69 63.98 ± 2.10 8.77 ± 1.61
a b a c
3.97 ± 0.37 3.84 ± 0.35 3.79 ± 0.41 1.17 ± 0.76
a a a b
45.61 43.02 40.78 4.37
12.85 12.79 11.57 14.21
0.373 0.367 0.424 0.106
a a a b
Total fecundity (eggs/female); oviposition rate (eggs/female/day); R0 (net reproductive rate in females/female); T (mean generation time in days); rm (intrinsic rate of increase in days1). Numbers within the same column followed by different letters are significantly different. * LSD test, P < 0.05. ** Student–Newman–Keuls test, P = 0.05.
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growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. The inability of phytoseiids to develop adequately when feeding on T. evansi has already been demonstrated for Euseius concordis (Chant) by Moraes and Lima (1983), for eight predatory mite species, including P. persimilis and N. californicus, by Moraes and McMurtry (1985), and more recently by Sarr et al. (2002) against this spider mite in Kenya. These studies revealed that none of the tested phytoseiid species were effective predators of the tomato spider mite. In all cases the oviposition and survival rates of predatory mites were low on this prey. Tetranychus evansi is an invasive species recently introduced into Spain, where it was first found on potato plants at the end of 1995 (Ferragut and Escudero, 1999). Since then, it has rapidly spread throughout the Spanish Mediterranean coast and the Canary Islands, causing considerable damage to tomato, aubergine, and potato plants, both outdoors and in greenhouses. Recent attempts to control the pest through mass releases of predatory mites, mainly P. persimilis, on tomatoes in some locations of the Mediterranean coast and the Canary Islands, have been unsuccessful. Plants may affect predatory mites through modifications of the suitability of its prey. Solanaceous plants produce secondary plant chemicals, like methil-ketones, and sesquiterpenes highly toxic for mites and insects (Chatzivasileiadis and Sabelis, 1997; Maluf et al., 2001). Poor efficacy of the predators in the present study may be due, at least in part, to the secondary plant compounds consumed while T. evansi was reared on potatoes. These possible effects may have caused a delay in protonymphal and deutonymphal development in both predatory mites. Furthermore, acquisition of secondary compounds by T. evansi may have affected predator reproduction through their act as feeding depressants as suggested by Moraes and McMurtry (1987) for P. persimilis and T. urticae reared on Solanum douglasi Dunal. Additional studies are needed to establish the reasons of the inefficiency of predatory mites on T. evansi and to determine whether phytoseiids are able to control the prey reared on other host than solanaceous plants. Tetranychus evansi continues to spread northwards up the Mediterranean coast and may already be found near the French border. In the absence of effective biological control agents, this species may soon threaten greenhouse crops in Central Europe. Its invasion of temperate protected crops may disrupt the ongoing efficient biological control program against T. urticae through mass releases of P. persimilis and N. californicus.
Acknowledgments The authors thank two anonymous referees for their useful comments on the first version of the manuscript.
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We are also grateful to Dr. Lourival Costa Paraı´ba from EMBRAPA, Meio Ambiente, Jaguariu´na, Sao Paulo (Brazil) for his assistance in life table data analysis. This research was funded by the Comisio´n Interministerial de Ciencia y Tecnologı´a (CICYT), Project AGF95-0826, and the Ministerio de Ciencia y Tecnologı´a (MCYT), Project AGL2003-05041.
References Amano, H., Chant, D.A., 1977. Life history and reproduction of two species of predacious mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni (Chant) (Acarina: Phytoseiidae). Canadian J. Zool. 55, 1978–1983. Ashihara, W., Hamamura, T., Shinkaji, N., 1978. Feeding, reproduction and development of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae) on various food substances. Bull. Fruit Tree Res. Stn. Japan E2, 91–98. Bakker, F.M., Klein, M.E., Mesa, N.C., Braun, A.R., 1993. Saturation deficit tolerance spectra of phytophagous mites and their phytoseiid predators on cassava. Exp. Appl. Acarol. 17, 97–113. Birch, L.C., 1948. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol. 17, 15–26. Chatzivasileiadis, E.A., Sabelis, M.W., 1997. Toxicity of methyl ketones from tomato trichomes to Tetranychus urticae. Exp. Appl. Acarol. 21, 473–484. Escudero, L.A., 1998. Estructura y dina´mica de las comunidades de a´caros del ecosistema hortı´cola mediterra´neo: bases para el empleo de fitoseidos en el control biolo´gico de las aran˜as rojas. Ph.D. Thesis. Universidad Polite´cnica de Valencia. (In Spanish). Escudero, L.A., Ferragut, F., 1998. Comunidades de a´caros del ecosistema hortı´cola mediterra´neo: composicio´n y distribucio´n geogra´fica. Bol. San. Veg., Plagas. 24, 749–762 (In Spanish). Escudero, L.A., Ferragut, F., 1999. Abundancia y dina´mica estacional de las poblaciones de fitoseidos en los cultivos hortı´colas valencianos (Acari: Tetranychidae, Phytoseiidae). Bol. San. Veg., Plagas. 25, 347–362 (In Spanish). Ferragut, F., Escudero, L.A., 1999. Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), una nueva aran˜a roja en los cultivos hortı´colas espan˜oles. Bol. San. Veg., Plagas. 25, 157–164 (In Spanish). Hamamura, T., Shinkaji, N., Ashihara, W., 1976. The relationship between temperature and developmental period, and oviposition of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae). Bull. Fruit Tree Res. Stn., Japan E1, 117–125. Helle, W., Sabelis, M.W. (Eds.), 1985. Spider Mites: Their Biology, Natural Enemies and Control, vol. 1B. World Crop Pests. Elsevier. Hulting, F.L., Orr, D.B., Obrycki, J.J., 1990. A computer program for calculation and statistical comparison of intrinsic rates of increase and associated life table parameters. Florida Entomol. 73, 601–612. Lenteren, J.C., van Woets, J., 1988. Biological and integrated pest control in greenhouses. Annu. Rev. Entomol. 33, 239–269. Lenteren, J.C., van Benuzzi, M., Nicoli, G., Maini, S., 1992. Biological control in protected crops in Europe. In: van Lenteren, J.C., Minks, A.K., de Ponti, O.M.B. (Eds.), In Biological Control and Integrated Crop Protection: Towards Environmentally Safer Agriculture. Pudoc Scientific Publishers, Wageningen, pp. 77–98. Lotka, A.J., 1924. Elements of Physical Biology. Williams & Wilkins, Baltimore, p. 460. Maluf, W.R., Canpos, G.A., Cardose, M.G., 2001. Relationships between trichome types and spider mite (Tetranychus evansi) repellence in tomatoes with respect to foliar zingiberene contents. Euphytica 121, 73–80.
384
L.A. Escudero, F. Ferragut / Biological Control 32 (2005) 378–384
McMurtry, J.A., 1991. Augmentative releases to control mites in agriculture. In: Dusbabek, F., Bukva, V. (Eds.), Modern Acarology, vol. 1. SPB Academic Publ., Prague, pp. 151–157, p. 651. Moraes, G.J., Lima, H.C., 1983. Biology of Euseius concordis (Chant) (Acarina: Phytoseiidae) a predator of the tomato russet mite. Acarologia 24, 251–255. Moraes, G.J., McMurtry, J.A., 1985. Comparison of Tetranychus evansi and T. urticae (Acari: Tetranychidae) as prey for eight species of phytoseiid mites. Entomophaga 30 (4), 393–397. Moraes, G.J., McMurtry, J.A., 1987. Physiological effect of the host plant on the suitability of Tetranychus urticae as prey for Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae). Entomophaga 32 (1), 35–38. Nihoul, P., 1992. Effect of temperature and relative humidity on successful control of Tetranychus urticae Koch by Phytoseiulus persimilis Athias-Henriot (Acari; Tetranychidae, Phytoseiidae) in tomato crops under glasshouse conditions. Med. Fac. Landbouww. Rijksuniv Gent. 57, 949–957. Overmeer, W.P.J., 1985. Rearing and handling. In: Helle, W., Sabelis, M.W. (Eds.), Spider Mites: Their biology, natural enemies and control. World Crop Pests. Elsevier.
Pratt, P.D., Coombs, E.M., Croft, B.A., 2003. Predation by phytoseiid mites on Tetranychus lintearius (Acari: Tetranychidae), an established weed biological control agent of gorse (Ulex europaeus). Biol. Control 26, 40–47. Sabelis, M.W., 1981. Biological control of two-spotted spider mites using phytoseiid predators. Part I: modelling the predator-prey interaction at the individual level. Agricultural Research Reports, Pudoc, Wageningen, p. 242. Sarr, I., Knapp, M., Ogol, C.K.P., Baumga¨rtner, J., 2002. Impact of predators on Tetranychus evansi Baker and Pritchard populations and damage on tomatoes (Lycopersicon esculentum Mill.) in Kenya. XI Int. Congress Acarology, Merida, Mexico. Abstract Book: 271. SPSS, 1999. SPSS Base 10.0 Application Guide. SPSS. Chicago. Stenseth, C., 1979. The effect of temperature and humidity on the development of Phytoseiulus persimilis and its ability to regulate populations of Tetranychus urticae (Acarina: Tetranychidae, Phytoseiidae). Entomophaga 24, 311–317. Takahashi, F., Chant, D.A., 1994. Adaptative strategies in the genus Phytoseiulus Evans (Acari: Phytoseiidae). II. Survivorship and reproduction. Int. J. Acarol. 20 (2), 87–96.