Sublethal effects of Beauveria bassiana on life table ...

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Sublethal effects of Beauveria bassiana on life table parameters of two–spotted spider mite, Tetranychus urticae (Acari: Tetranychidae) a

a

Farzaneh-Sadat Seyed-Talebi , Katayoon Kheradmand , Reza b

Talaei-Hassanloui & Khalil Talebi-Jahromi

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Department of Plant Protection, College of Abureyhan, University of Tehran, Pakdasht, Iran b

Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran Available online: 17 Jan 2012

To cite this article: Farzaneh-Sadat Seyed-Talebi, Katayoon Kheradmand, Reza Talaei-Hassanloui & Khalil Talebi-Jahromi (2012): Sublethal effects of Beauveria bassiana on life table parameters of two–spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), Biocontrol Science and Technology, 22:3, 293-303 To link to this article: http://dx.doi.org/10.1080/09583157.2012.655709

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Biocontrol Science and Technology, Vol. 22, No. 3, March 2012, 293303

RESEARCH ARTICLE Sublethal effects of Beauveria bassiana on life table parameters of two spotted spider mite, Tetranychus urticae (Acari: Tetranychidae)

Farzaneh-Sadat Seyed-Talebia*, Katayoon Kheradmanda, Reza Talaei-Hassanlouib and Khalil Talebi-Jahromib a

Department of Plant Protection, College of Abureyhan, University of Tehran, Pakdasht, Iran; Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

Downloaded by [Farzaneh-Sadat Seyed-Talebi] at 00:59 23 April 2012

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(Received 24 August 2011; final version received 5 January 2012) Effects of the entomopathogenic fungus Beauveria bassiana were studied on life table parameters of two-spotted spider mite, Tetranychus urticae feeding on bean and cucumber under laboratory conditions. The developmental periods for all immature stages were not affected by fungal infection on each host plant but the duration of larval stage was significantly longer on bean. The female and male longevity, oviposition period and fecundity were significantly lower on fungustreated mites but were not different between two host plants. Significant reductions were found on the intrinsic rate of increase (rm), the net reproductive rate (R0), the finite rate of increase (l), the mean generation time (Tc) and the population doubling time (Dt) as a result of mycosis. Only the mean generation time (Tc) was influenced considering the effect of host plant, which was shorter on cucumber. Keywords: Beauveria bassiana; sublethal effect; life table; Tetranychus urticae; host plant

Introduction The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is one of the most serious cosmopolitan phytophagous mites, commonly found on many horticultural and agricultural crops (Bolland, Gutierrez, and Flechtmann 1998; Tsagkarakou, Pasteur, Cuany, Chevillon, and Navajas 2002). Synthetic chemical acaricides are generally utilised against this mite, as they are easy-to-apply, effective and economical (Ay and Yorulmaz 2010). Long-term overuse of chemical pesticides for pest control may have resulted in spider mite resurgence and subsequent high-level resistance to common acaricides and leading to growing concern about environmental and health risks associated with their use (Gerson and Cohen 1989; Ambikadevi and Samarjit 1997; Stumpf, Zebitz, Kraus, Moores, and Nauen 2001; Maniania, Bugeme, Wekesa, Delalibera, and Knapp 2008). These problems have led to the use of alternative strategies, one which is microbial control using fungi (Chandler et al. 2000; Van der Geest, Elliot, Breeuwer, and Beerling 2000). Enthomopathogenic fungi often play an important role in the regulation of natural mite populations and are sometimes able to decimate *Corresponding author. Email: [email protected] ISSN 0958-3157 print/ISSN 1360-0478 online # 2012 Taylor & Francis http://dx.doi.org/10.1080/09583157.2012.655709 http://www.tandfonline.com


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populations (Van der Geest et al. 2000). Among these fungi, Beauveria bassiana (Bals.) Vuill. seems to be a good candidate for controlling sucking pests, such as aphids, leafhoppers, whiteflies and mites (Hatting, Poprawski, and Miller 2000; Faria and Wraight 2001; Vandenberg et al. 2001; Feng et al. 2004; Wekesa, Knapp, Maniania, and Boga 2006; Maniania et al. 2008; Bugeme, Maniania, Knapp, and Boga 2008; Seiedy, Saboori, Allahyari, Talaei-Hassanloui, and Tork 2010). Commercial products have been developed with this fungus with successful results (Faria and Wraight 2001). Not much research has been conducted to study sublethal effects of fungi on life table parameters of spider mites (Wekesa et al. 2006; Shi and Feng 2009), while sublethal effects of fungal infection can have important implications for the population dynamics of the host, which ultimately contributes to the status of the target insect as a pest (Arthurs and Thomas 2000; Blanford and Thomas 2001). However, the host plant species can affect the susceptibility of herbivorous arthropods to entomopathogenic fungi (Santiago-Alvarez, Maranhao, Maranhao, and Quesada-Moraga 2005; Olleka, Mandour, and Ren 2010). According to importance of life table studies in population ecology (Sakai et al. 2001) and pest control timing studies (Chi 1990), information about sublethal effects of pathogens on these parameters with consideration of host plant effects would be useful in development of predictive epizootiological models and successful biological control programs. Thus, we attempted to study sublethal effects of B. bassiana on life table parameters of T. urticae, feeding on bean and cucumber. This information can provide insights into the long-term effects of applied fungal formulations on spider mite populations.

Materials and methods Plants and mites The host-plants, cucumber (Cucumis sativus L. cv. Negin) and bean (Phaseolus vulgaris L.), were grown in plastic pots and maintained in the greenhouse at 25938C, 65920% RH and a photoperiod of 16:8 (L:D) h. Spider mites were collected from a glasshouse in Karaj and maintained either on bean or cucumber plants at 25918C; 70910% RH and a photoperiod of 16:8 (L:D) h for several generations.

Fungus A native strain of B. bassiana EUT105 (soil origin) was grown on Sabouraud Dextrose Agar (SDA) medium and maintained at 25918C, 70910% RH and a photoperiod of 16:8 (L:D) h. Cultures were scraped after sporulation and conidia were obtained (Goettel and Inglis 1997). Dry conidia were suspended in 0.02% Tween 80 in water and diluted to 1 108 conidia/ml.

Effect of fungal infection on life table parameters To assess development and life table parameters of T. urticae on each host plant, a 20-mm diameter leaf disk of each plant was placed on wet cotton wool in 90-mm


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diameter Petri dishes and one newly emerged mite larva was introduced. The mite was sprayed with 1.5 ml of a suspension of fungal conidia using a Potter spray tower (Burkard, UK) with 0.7 kg/cm2 pressure. The controls were treated with distilled water 0.02% Tween 80. Each treatment consisted of 50 replicates for fungus and 25 replicates for the control. The treated leaf disks were air-dried for 30 min, and then the Petri dishes placed in an incubator at 25918C, 70910% RH, and a photoperiod of 16:8 (L:D) h. Twenty four hours later, the lids were replaced with lids which had a hole of 3 cm diameter in the center. Leaf disks were replaced with fresh leaves every 3 days to avoid food source contamination. For each treatment, the developmental time and survivorship at all immature stages as well as adult longevity were recorded every 24 h. For the dead mites, a mycosis test was carried out on wet filter paper. After emergence of a female, one male was introduced to the leaf disk. The number of laid eggs by each female was recorded daily until the last female died.

Data analysis The life history raw data of all individuals were analysed based on the age-stage, two-sex life table theories (Chi and Liu 1985) and the method described by Chi (1988). The standard errors of the life table parameters were estimated using the Jackknife method (Sokal and Rohlf 1995). The computer program TWOSEX-MS Chart (Chi 2005) was used for data analysis and Jackknife estimation. The developmental time for immature stages and female and male adult longevity, the reproductive period and the total female fecundity, the age-specific survival rate (lx), the age-specific fecundity (mx) and the population parameters (the intrinsic rate of increase from the Euler-Lotka equation: S e-rm(x1) lxmx 1; finite rate of increase lerm; net reproduction rate R0 S lxmx the mean generation time Tc (ln R0)/rm were calculated accordingly. The population doubling time Dt was calculated using formula Dt (ln 2)/rm.The Student’s t-test was used to determine differences in population parameters (P 0.05), developmental times and fecundities between two different treatments. All the analyses were done using SAS 9.1 (SAS Institute 2002).

Results The developmental time and longevity The developmental period for B. bassiana treated mites was not significantly different from the controls at all immature stages (larva, protonymph and deutonymph) on bean and cucumber (Tables 1 and 2). Only the duration of larval stage was significantly different between the two host plants and was longer on bean than on cucumber (t98 66.31, P 0.0001). The longevity of the emerged adult females and males was significantly affected by fungal infection. The highest value for the longevity of females was 1090.23 days in the bean control treatment whereas the lowest value, 6.690.12 days was recorded for fungus-treated mites on beans. Difference in longevities of the treated females was not statistically different between two host plants (t78 1.04, P0.30). Through the mycosis test, mycelial growth was revealed on dead mite body surfaces.

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Table 1. Mean (9SE) of developmental time for juvenile stages and adult longevity of Tetranychus urticae on bean.


Statistics Developmental time Larva Protonymph Deutonymph Total pre-adult duration Adult longevity Female Male

Untreated mites (mean9SE)

Treated mites (mean9SE)

t

d.f.

P

3.090.2 1.090.2 1.090.2 8.090.3

3.090.4 1.090.4 1.090.3 8.090.5

0.06 0.04 1.48 0.79

73 73 73 73

0.95 0.96 0.14 0.43

10.090.2 7.390.3

6.690.1 6.190.1

14.62 5.56

58 13

B0.0001* B0.0001*

*Significant difference (Student’s t-test, P B 0.05).

Reproductive potential There were significant differences among B. bassiana-treated and untreated mites for oviposition period and fecundity (Tables 3 and 4). The mean number of eggs laid by a single untreated female was 30.691.2 and 2991 on bean and cucumber, respectively compared to 18.390.9 and 17.290.9 eggs/female in B. bassiana treated mites. Furthermore, the oviposition period for untreated mites was significantly lower than that of treated mites on each host plant. Neither the oviposition period (t78 1.12, P 0.26) nor the fecundity (t78 0.90, P0.37) differed significantly among the two host plants.

Age-specific survival rates (lx) and age-specific fecundity (mx) The values of age-specific survival rates (lx) and age-specific fecundity (mx) on each host plant are presented in Figures 14. Maximum values of survival rates were for immature stages. Adults were the most susceptible to fungal infection ages. The untreated mites lived 20 and 18 days on bean and cucumber while all treated mites Table 2. Mean (9SE) of developmental time for juvenile stages and adult longevity of Tetranychus urticae on cucumber. Statistics Developmental time Larva Protonymph Deutonymph Total pre-adult duration Adult longevity Female Male



t

d.f.

P

2.190.6 1.090.5 1.090.3 7.190.1

2.090.3 1.090.2 1.090.3 7.190.5

1.77 1.46 0.35 1.67

73 73 73 73

0.08 0.14 0.72 0.09

8.990.3 6.890.2

6.890.1 5.390.2

8.16 4.16

59 12

B0.0001* B0.0001*



297

Table 3. Mean (9SE) of reproductive period and fecundity of Tetranychus urticae on bean. Statistics Reproductive period Pre-oviposition period Oviposition period Post-oviposition period Total fecundity



t

d.f.

P

0.790.1

0.890.04

0.64

58

0.52

8.591.3 1.290.1

5.390.1 1.490.1

14.77 1.81

58 58

B0.0001* 0.07

30.691.2

18.390.9

8.52

58

B0.0001*



died by day 16. The highest and the lowest values of age-specific fecundity (mx) were 6 (eggs/female/day) for control mites on cucumber and 4.2 (eggs/female/day) for infected mites on bean.

Life-table parameters The demographic parameters of T. urticae were found to be significantly influenced by infection of B. bassiana (Tables 5 and 6). Untreated mites had higher rm values on cucumber (0.2690.009 female/female/day) and on bean (0.2490.007 female/female/ day) than the treated mites on cucumber (0.2390.007) and bean (0.2190.006). Reduction of the net reproductive rate (R0), the finite rate of increase (l), the mean generation time (Tc) and the population doubling time (Dt) on each host plant indicated that fungus-treated mite population developed slower than the control population. The effects of two host plants on life-table parameters were not statistically significant, though Tc of T. urticae on cucumber was shorter than on the bean (t98 7.21, P B0.0001).

Discussion Although the effect of B. bassiana on reproductive potential of T. urticae was demonstrated by Shi and Feng (2009), ours is the first comprehensive study on Table 4. Mean (9SE) of reproductive period and fecundity of Tetranychus urticae on cucumber. Statistics Reproductive period Pre-oviposition period Oviposition period Post-oviposition period Total fecundity



t

d.f.

P

0.790.1

0.990.02

3.26

59

0.001*

7.791.2 1.29 0.1

5.590.9 1.490.1

10.97 1.50

59 59

B0.0001* 0.12

2991.0

17.290.9

8.30

59

B0.0001*



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Figure 1. The change process of lx and mx curves for untreated mites on bean.

sublethal effects of B. bassiana on life table parameters of T. urticae considering host plant effects as well. According to our results, fungal treatment had no effect on developmental time of immature stages, which is in accordance with Zhou, Ali, and Huang (2010) who concluded that sub-lethal doses of Isaria fumosorosea (Wize) Brown and Smith had no effects on developmental time of Axinoscymnus cardilobus (Ren and Pang) (Coleoptera: Coccinellidae). However, in contrast, Hafez, Zaki, Moursy, and Sabbour (1994) showed the duration of treated pupae of Phthorimae operculella (Zeller) (Lepidoptera: Gelechiidae) was longer because of infection by B. bassiana. The different results probably occurred due to different plant nutritional quality of the host plants and morphological or allelochemical features (Agrawal 2000; Pietrosiuk, Furmanowa, Kropczynska, Kawka, and Wiedenfeld 2003; Balkema-Boomstra et al. 2003).

Figure 2. The change process of lx and mx curves for treated mites on bean.



299

Figure 3. The change process of lx and mx curves for untreated mites on cucumber.

Developmental periods of mite larvae were different on two host plants as previously demonstrated by Razmjou, Tavakkoli, and Nemati (2009) and Praslicka and Huszar (2004). The adult longevity, reproductive period and fecundity were lower on fungus-treated mites than the controls while the host plant had no significant effect on theses parameters. Reduction in fecundity and survival time of T. urticae was similarly reported by Shi and Feng (2009) due to infection by B. bassiana, I. fumosorosea and Metarhizium anisopliae (Metchnikoff). The age-specific survival rate (lx) showed that immature stages were less susceptible to infection by B. bassiana than adults; the values of survival rate (lx) for these stages were similar with controls. This differential susceptibility at various life stages may be related to molting of immature mites. Ecdysis has been reported to be an important factor in host resistance to fungal infection, particularly when the time interval between successive moltings is short (Vey and Fargues 1977).Whereas T. urticae has three immature stages (larva, protonymph and deutonymph) and our

Figure 4. The change process of lx and mx curves for treated mites on cucumber.

300


Table 5. Values of life-table parameters for Tetranychus urticae on bean. Parameter rm l R0 Tc Dt



d.f.

t

P

0.2490.007 1.2790.09 25.6892.48 13.4790.14 1.4990.04

0.2190.007 1.2490.08 14.391.28 12.3790.09 1.2890.06

73 73 73 73 73

2.29 2.33 4.54 6.63 2.30

0.024* 0.013* B0.0001* B0.0001* 0.024*



experiment showed that the time interval of each molting is short (13 days, SeyedTalebi and Talaei-Hassanloui unpublished data), conidia may be shed before being able to penetrate the cuticle (Gatarayiha, Laing, and Miller 2009). Our results are in agreement with Irigaray, Marco-Mancebon, and Perez-Moreno (2003) and Gatarayiha et al. (2009) who showed that B. bassiana had a greater effect on adult female T. urticae than immature stages. The intrinsic rate of increase (rm) is the most important parameter for describing the growth potential of a pest population under different conditions, as it reflects an overall effect on development, reproduction and survival (Southwood and Henderson 2000). In the present work, values of (rm) were found to be significantly lower on treated mites. Huang, Ali, Ren, and Wu (2010) reported that I. fumosorosea had effect on rm of B. tabaci and Plutella xylostella (Linnaeus) (Lepidoptera: Plutellidae). Our results showed that the host plant had no influence on sublethal effect of B. bassiana because values of (rm) were not significantly different on infected mites on bean and cucumber. Only the mean generation time (Tc) was different between two host plants and treated mites lived longer on bean. However, it is notable that other factors, for example, temperature (Wermelinger, Oertli, and Baumgartner 1991; Krips, Witul, Willems, and Dicke 1998; Bounfour and Tanigoshi 2001; Praslicka and Huszar 2004), humidity (Boudreaux 1958), affect development, fecundity and consequently population parameters. The adult stage is probably the most damaging stage of T. urticae because of its longevity and feeding rate. Reduction in the adult population may mean a reduction in the rate of population build-up of the mite, as fewer progeny and consequently less number of generations are produced per season. Our results demonstrated that this isolate of B. bassiana affected fecundity and life Table 6. Values of life-table parameters for Tetranychus urticae on cucumber. Parameter rm l R0 Tc Dt



d.f.

t

P

0.2690.009 1.3090.012 23.1692.49 11.9590.08 1.1890.05

0.2390.006 1.259 0.08 14.2291.17 11.5190.07 1.3890.05

73 73 73 73 73

2.82 2.86 3.74 3.70 2.41

0.006* 0.005* 0.0004* 0.0004* 0.018*



301

table parameters of T. urticae. Consequently, it may have good potential as a biological agent for management of two- spotted spider mites. Acknowledgements This publication is a part of the first author’s M.Sc. thesis funded by the University of Tehran and Center of Excellence for Biological Control of Plant Pests, which we thank for their financial support. Mahmood Fazeli was greatly acknowledged for his technical help.


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