- Email: [email protected]
Studies on life cycle of mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), on different hosts at different constant temperatures
Crop Protection 30 (2011) 1553e1556
Contents lists available at SciVerse ScienceDirect
Crop Protection journal homepage: www.elsevier.com/locate/cropro
Studies on life cycle of mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), on different hosts at different constant temperatures Satish V. Patila, b, *, Chandrashekhar D. Patila, Rahul B. Salunkhea, Vijay L. Maheshwaria, Bipinchandra K. Salunkea a b
School of Life Sciences, North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India North Maharashtra Microbial Culture Collection Centre (NMCC), North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 May 2011 Received in revised form 12 August 2011 Accepted 16 August 2011
The life cycle of a laboratory reared parthenogenic line of mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) was investigated on six host plants (Lagenaria siceraria var.clavata, Solanum tuberosum L. var. Kufri Chandramukhi, Praecitrullus fistulosus (Stocks) Pangalo var. MTNH1, Cucurbita pepo var. Styriaca, Triticum aestivum L. var. Lokvan, H. rosa sinensis L.) at five constant temperatures (25, 29, 35, 38, 42 C). The number of emerging crawlers and adults as well as weight of adults varied with host and temperature. P. fistulosus and H. rosa sinensis were suitable hosts for laboratory rearing of M. hirsutus. However, ease of maintenance of P. fistulosus to produce M. hirsutus under laboratory conditions is an additional advantage compared to using green plants such as H. rosa sinensis. Among the range of constant temperatures, 38 C was found to be the most favourable for the development and survival of M. hirsutus. These results suggest that P. fistulosus fruits are suitable hosts for laboratory rearing and life cycle studies of M. hirsutus. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Laboratory rearing Longevity Praecitrullus fistulosus Hibiscus rosa-sinensis Crawler
1. Introduction Mealybugs (Hemiptera: Pseudococcidae) are plant sap-sucking insects that constitute a family with about 2000 species, some of which are major pests of agricultural plants (Williams, 1985; Gullan and Kosztarab, 1997). The pink hibiscus mealybug, Maconellicoccus hirsutus (Green) was first described as Phenacoccus hirsutus Green based on specimens collected in India on an undetermined shrub (Green, 1908). Ezzat (1958) re-described the species as M. hirsutus. The species is native to southern Asia, and has spread to other parts of the world such as Africa, and more recently North America and the Caribbean, where the range is still extending (Kairo et al., 2000). It attacks more than 200 plants, trees and shrubs with host records extending to 76 families, with some preference for Fabaceae, Malvaceae and Moraceae (Mani, 1989; Garland, 1998). M. hirsutus has been recorded causing economic damage to many crops including avocado, Persea americana Mill, cotton, Gosspium hirsutum L., peanut, Arachis hypogaea L., nursery crops, soya bean, Glycine max (L.) Merrill, and vegetables (Moffitt, 1999). The annual cost of control and * Corresponding author. School of Life Sciences, North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India. Fax: þ91 257 2258403. E-mail addresses: [email protected] (S.V. Patil), bipin_salunke@yahoo. com (B.K. Salunke). 0261-2194/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.08.010
damages from invasion of M. hirsutus into US agriculture has been estimated at $750 million per year in the absence of control measures, with the global total being $5 billion (Moffitt, 1999; ARS, 2003). In India, losses have been reported for cotton (Muralidharan and Badaya, 2000), the fibre crops roselle, Hibiscus sabdariffa L., Kenaf, Hibiscus cannabinus L., and Boehmeria nivea L. (Ghose, 1972; Raju et al., 1988), grapevine, Vitis vinifera L. (Manjunath, 1985), pigeonpea, Cajanus cajan L. Millsp. (Patel et al., 1990), and Zizyphus mauritiana Lamarck (Balikai and Bagali, 2000). Despite the economic importance of M. hirsutus, there is a lack of detailed life history data on the species. Life tables and developmental rates are essential tools for investigating and understanding the impact of temperature on growth, survival, reproduction and rate of increase of an insect population. Life tables are especially important in understanding age dynamics of adult populations studied under controlled laboratory conditions (Carey, 2001) and in tackling the issue of life expectancy when affected by environmental changes (Pilkington and Hoddle, 2007). Biological control of mealybugs by laboratory rearing and releases of natural enemies in the field has been successful against a number of pseudococcid pests (Walton and Pringle, 2002). For rearing natural enemies of mealybugs such as the predatory beetles Cryptolaemus montrouzieri Mulsant and Schymnus coccivora Ramkrishna (Coleoptera: Coccinellidae), and the parasitoid, Anagyrus
1554
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
kamali Moursi (Hymenoptera: Encyrtidae) (Cross and Noyes, 1998), food plants and fruits that lead to high population growth rates of mealybugs need to be identified and exploited for laboratory rearing and production of biocontrol agents. However, there is not enough documented evidence about host suitability for rearing of M. hirsutus and its natural enemies (Johnson, 2010). Earlier reports on the life history of M. hirsutus were conducted at either a single constant temperature (Persad and Khan, 2002; Serrano and Lapointe, 2002) or fluctuating temperature regimens (Babu and Azam, 1987). Temperature is known to affect multiple biological traits such as sex ratio, adult life-span, survival, fecundity and fertility of insects including Bactrocera doralis Hendel, Clavigralla tomentosicollis Stål and Clavigralla shadabi Dolling (Singh and Ashby, 1985; Yang et al., 1994; Dreyer and Baumgartner, 1996). At low temperature, development occurs at a slower rate than at high temperature (Jarosik et al., 2004). It has been estimated that with a 2 C temperature increase insects might experience one to five additional life cycles per season (Yamamura and Kiritani, 1998). In this study, we examine the effects of different hosts and five constant temperatures (25e42 C) on the development of M. hirsutus. 2. Materials and methods A colony of M. hirsutus was initiated in February 2009 with adult females collected from an infested cotton field in the Jalgaon region of Maharashtra state, India. Samples were examined under a binocular dissection microscope in the laboratory. The life stages of M. hirsutus were identified using Hall (1926) and Meyerdirk et al. (1998). The colony of M. hirsutus was reared on Praecitrullus fistulosus (Stocks) Pangalo, as described by Patil et al. (2010). The colony was maintained by releasing one female per P. fistulosus fruit kept in glass trays (25 15 cm) at 30 2 C, 70 5% RH, and 16:8 h light: dark photoperiod. The fruits [Lagenaria siceraria (Mol.) Standley var.clavata (dudhi), Solanum tuberosum L. (sprouted potato) var. Kufri Chandramukhi, P. fistulosus (Stocks) Pangalo var. MTNH1 (tinda), Cucurbita pepo var. Styriaca (pumpkin)] were obtained from a supermarket, washed in tap water to ensure the removal of pesticide residues, dried and checked for prior infestation with insects. The fruits were kept in glass trays. Hibiscus rosa-sinensis L. obtained from a local nursery and 28 day old laboratory grown wheat, Triticum aestivum L. var. Lokvan, were used as the host plants for M. hirsutus. One gravid female per fruit in tray or per seedling in pot was released at 37.0 1.0 C and 70 5% relative humidity in an environmental chamber (REMI instruments, CHM 12S, India). The experiment continued until the death of the adult female on the host. Life cycle at each treatment was monitored by recording the
number of eggs, crawlers and adults using a stereomicroscope. The average weight of ten adult insects per fruit or seedling was recorded using an electronic balance (Shimadzu, LIBROR, AEG-120, Japan). The influence of five constant temperatures 25, 29, 35, 38, and 42 1.0 C at 70 5% relative humidity was examined on the cumulative growth of M. hirsutus in an environmental chamber (REMI instruments, CHM 12S, India). One gravid female was released per P. fistulosus in tray. The experiment continued until the death of the adult female on the host. Life cycle at each treatment was monitored by recording the number of eggs, crawlers, adults and the weight. Every experiment had three replicates of a fruit per tray or seedling per pot. The data were analysed by one way analysis of variance (ANOVA) using statistical software Minitab for Windows version 13. Treatment means were separated by Tukey’s multiple comparison test at a ¼ 0.05. 3. Results Hibiscus rosa sinensis was found to be the most suitable host (Table 1) with the highest number of eggs, crawlers and adults along with greater longevity (time from egg hatch to death of adult). Fruits of P. fistulosus were found to be the second most suitable host after H. rosa sinensis. Hosts C. pepo (93%), L. siceraria (73%), S. tuberosum (33%) and T. aestivum (29%) had fewer eggs as compared to P. fistulosus, thus resulting in reduced subsequent cumulative survival. The longevity of adult females was similar when reared on P. fistulosus, C. pepo and H. rosa sinensis, at close to 21 days. Female longevity was significantly shorter by 8.7 days on T. aestivum, 6.3 days on S. tuberosum and 2.3 days on L. siceraria compared to P. fistulosus (Table 1). Females reared on C. pepo, H. rosa sinensis and P. fistulosus produced significantly more eggs than females reared on other hosts (Table 1). However, the number of eggs obtained on sprouted potato and wheat were 67 and 71% fewer, respectively, than on P. fistulosus. The mean percentage of adult emergence from laid eggs was found to be highest for females reared on P. fistulosus (41.2%) and H. rosa sinensis (41.5%). Moderate adult emergence was obtained for females reared on C. pepo (30.0%) and L. siceraria (28.5%), whereas the lowest adult emergence was observed for S. tuberosum (20.6%), followed by T. aestivum (11.3%). Females reared at 25 C and 42 C produced significantly fewer eggs and reduced numbers of crawlers, adults, adult weight and longevity (Table 2). The egg production, number of crawlers and adult formation increased with temperature until 38 C. The developmental time also decreased with an increase in temperature from 25 to 42 C.
Table 1 Life cycle of the mealybug, Maconellicoccus hirsutus on different hosts.a Hosts
Number of eggs
Number of crawlers
Dudhi (Lagenaria siceraria var.clavata) Sprouted potato (Solanum tuberosum L. var. Kufri Chandramukhi) Tinda (Praecitrullus fistulosus(Stocks) Pangalo var. MTNH1) Pumpkin (Cucurbita pepo var. Styriaca) Wheat plant (Triticum aestivum L. var. Lokvan) Hibiscus plant (H. rosa sinensis L.) F df P
202.00 (1.00) d 92.33 (1.53) e
161.33 (2.08) d 55.33 (1.53) e
57.67 (1.53) d 19.00 (2.00) e
18.67 (0.58) b 14.67 (0.58) c
278.33 (1.53) b
225.00 (2.00) b
114.67 (2.08) b
21.00 (1.00) a
258.67 (1.15) c 79.67 (1.53) f 302.00 (1.00) a 16036.24 5, 12 <0.0001
216.00 (3.61) c 38.67 (4.51) f 268.33 (2.08) a 3334.75 5, 12 <0.0001
77.67 (1.53) c 9.00 (1.00) f 125.33 (1.53) a 2544.28 5, 12 <0.0001
21.00 (1.00) a 12.33 (0.58) d 21.00 (1.00) a 63.53 5, 12 <0.0001
Data are presented as mean (SD). Means within a given column followed by the same letter are not significantly different, Tukey’s MRT, (a ¼ 0.05). a One female was released on each host.
Number of Adults
Time (Days)
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
1555
Table 2 Effect of different constant temperatures on the life cycle of the mealybug, Maconellicoccus hirsutus.a Treatment ( C)
Number of eggs
Number of crawlers
Number of adults
Weight of adults (mg)
Longevity (Days)
25 29 35 38 42 F df P
74.00 (1.00) 155.33 (1.53) 222.33 (1.53) 272.67 (1.53) 76.00 (2.00) 9704.06 4, 10 <0.0001
55.33 (1.53) 132.67 (1.15) 181.67 (1.53) 246.00 (1.00) 43.00 (1.00) 13716.40 4, 10 <0.0001
12.00 (1.00) 35.67 (1.53) 85.67 (1.53) 112.33 (1.53) 16.00 (1.00) 3306.57 4, 10 <0.0001
3.87 (0.12) 4.00 (0.10) 5.30 (0.10) 5.67 (0.12) 3.73 (0.06) 242.93 4, 10 <0.0001
22.33 (0.58) 20.33 (1.15) 19.33 (0.58) 19.33 (0.58) 18.00 (0.00) 16.64 4, 10 <0.0001
d c b a d
d c b a e
e c b a d
c c b a c
a b bc bc c
Data are presented as mean (SD). Means within a given column followed by the same letter are not significantly different, Tukey’s MRT, (a ¼ 0.05). a One female was released on each Praecitrullus fistulosus.
4. Discussion P. fistulosus fruits are reported here for the first time for laboratory rearing of M. hirsutus. This host produced a large number of insects with the same developmental rate and a high survival rate when compared to previously used hosts such as C. pepo, S. tuberosum and Cucurbita moschata (Duchesne) cv. Chirimen (Serrano and Lapointe, 2002). H. rosa sinensis is a host plant frequently found with natural infestations of M. hirsutus (Persad and Khan, 2007; Tanwar et al., 2007). Wheat has been reported as an incidental host on which crawlers were able to establish and produce injury symptoms (Dhawan, 2007). Our study showed that M. hirsutus could complete their life cycle and reproduce on wheat in the laboratory. However, the weak performance of M. hirsutus on wheat reduces its suitability as a host for laboratory rearing. The difference in fecundity of M. hirsutus on different host plant species or food substrates is supported by earlier reports where Serrano and Lapointe (2002) obtained the highest mean fecundity when the females were reared on Japanese pumpkin (C. moschata) (162 eggs) and the lowest on a meridic diet (59 eggs). Other reports of M. hirsutus fecundity varied greatly from 84 to 654 eggs on Hibiscus sabdariffa L. as reported by Ghose (1972) and 386e540 eggs on V. vinifera L. as reported by Mani (1986). Most of the previous studies are from countries where average field temperatures are below 30 C. In the present study area (Jalgaon, 21 050 N 75 400 E, Elevation 218 masl), there are two distinct seasons, NovembereMarch (winter - average temperature 7e25 C) and AprileOctober (summer - average temperature 23e45 C). The temperatures in our study are within the average field conditions in India. Seasonal climatic patterns influence mealybug populations. In the field, we observed that mealybug infestation increased with temperature. This prompted us to study the effect of a range of temperatures on the life cycle performance of mealybugs in a laboratory setting. Research reports from the Caribbean (Kairo et al., 2000), South India (Mani and Thontadarya, 1989) and Australia (Goolsby et al., 2002) showed that populations were low during the rainy season and winter, and peaked during the summer months. In the present study, we also found that increased temperature accelerated the development of female M. hirsutus. Previous reports by other researchers also reported an increased developmental rate with temperature up to 27 C (Serrano and Lapointe, 2002; Babu and Azam, 1987). At lower temperatures, reduced development would be expected primarily because the immature stages convert less food into body tissue, resulting in low growth and thus longer developmental times (Atkinson and Sibly, 1997). In contrast, Chong et al. (2008) reported production of 260e300 eggs by M. hirsutus reared on hibiscus plant cuttings at 20e27 C, but only 100 eggs at 30 C and occurrence of complete development in 29 days at 27 C. An ideal host for the rearing of M. hirsutus should produce adults within a short development time. Females should be able to produce
large ovisacs with a high survival rate of offspring. P. fistulosus fruits have the added advantage of being convenient for the application of insecticidal test materials to carry out bioefficacy assays (Patil et al., 2010), and are easy to handle for the measurement of the number of eggs, crawlers and adults. P. fistulosus fruits are an easily available, cheap source of host material for rearing of mealybugs. In this study, we demonstrated that the most suitable rearing temperature for M. hirsutus was 38 C. The investigations can be exploited for laboratory rearing and production of biocontrol agents of mealybugs such as predatory beetles and the parasitoids at different temperature range in diverse areas. In addition to this, the study can help to determine the conditions in the field that maximize the efficacy of biocontrol agents of mealybugs. Similarly, different strains of pest and natural enemies need to be studied from areas with varying environmental conditions.
Acknowledgement Financial assistance from the Department of Biotechnology, New Delhi, in the form of a project grant (2010e2013) is gratefully acknowledged [BT/PR 12694/AGR/05/474/(letter I)].
References ARS, 2003. On the Lookout for Scaly Invaders. URL. http://www.ars.usda.gov/is/AR/ archive/dec03/scaley1203.pdf. Atkinson, D., Sibly, R.M., 1997. Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol. Evol. 6, 235e239. Babu, T.R., Azam, K.M., 1987. Studies on biology, host spectrum and seasonal population fluctuation of the mealybug, Maconellicoccus hirsutus Green on grapevine. Indian J. Hortic. 44, 284e288. Balikai, R.A., Bagali, A.N., 2000. Population density of mealy bug, Maconellicoccus hirsutus on ber (Zizyphus mauritiana) and economic losses. Agri. Sci. Dig. 20, 62e63. Carey, J.R., 2001. Insect biodemography. Annu. Rev. Entomol. 46, 79e110. Chong, J.H., Amy, L.R., Catharinem, M.M., 2008. Life history of the mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), at constant temperatures. Environ. Entomol. 37, 323e332. Cross, A.E., Noyes, J.S., 1998. Dossier on Anagyrus kamali Moursi an Exotic Natural Enemy for Biological Control of the Hibiscus Mealybug in the Caribbean. International Institute of Biological Control, Trinidad and Tobago, 26 pp. Dhawan, A.K., 2007. Status of Mealy Bug in Punjab. URL. http://www.ncipm.org.in/ MealybugPunjab.doc. Dreyer, H., Baumgartner, J., 1996. Temperature influence on cohort parameters and demographic characteristics of the cowpea coreids Clavigralla tomentosicollis and C. shadabi. Entomol. Exp. Appl. 78, 201e213. Ezzat, Y.M., 1958. Maconellicoccus hirsutus (Green), a new genus, with redescription of the species [Homoptera: Pseudococcidae-Coccoidea]. Bull. Entomol. Soc. Egypt. 42, 377e383. Garland, J.A., 1998. Pest Risk Assessment of the Pink Mealy Bug Maconellicoccus hirsutus (Green), with particular reference to Canadian Greenhouses. PRA 96e21. Canadian Food Inspection Agency, Ottawa (CA). Ghose, S.K., 1972. Biology of the mealybug, Maconellicoccus hirsutus Green (Pseudococcidae: Hemiptera). Indian Agric. 16, 323e332. Goolsby, J.A., Kirk, A.A., Meyerdirk, D.E., 2002. Seasonal abundance and natural enemies of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Australia. Fla. Entomol. 85, 494e498.
1556
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
Green, E.E., 1908. Remarks on Indian scale insects (Coccidae), Part III. With a catalogue of all species hitherto recorded from the Indian continent. Mem. Dep. Agric. India Ent. Ser. 2, 15e46. Gullan, P.J., Kosztarab, M., 1997. Adaptations in scale insects. Annu. Rev. Entomol. 42, 23e50. Hall, W.J., 1926. The Hibiscus mealybug (Phenacoccus hirsutus, Green) in Egypt in 1925 with notes on the introduction of Cryptolaemus montrouzieri, Muls. Ministry of Agriculture, Egypt. Tech. Scientific Serv. Bull. No. 70, 1e15. Jarosik, V., Kratochvil, L., Honek, A., Dixon, A.F.G., 2004. A general rule for the dependence of developmental rate in ectothermic animals. Proc. R. Soc. B 271 (Suppl.), S219eS221. Johnson, T., 2010. Biology of the Oleander mealybug, Paracoccus burnerae (brain) (hemiptera: pseudococcidae). M.Sc. Thesis, University of Stellenbosch, South Africa. Kairo, M.T.K., Pollard, G.V., Peterkin, D.D., Lopez, V.F., 2000. Biological control of the hibiscus mealy bug, Maconellicoccus hirsutus in the Caribbean. Int. Pest Manag. 5, 241e254. Mani, M., 1986. Distribution, bioecology and management of the grape mealybug (Maconellicoccus hirsutus Green) with special reference to its natural enemies. PhD dissertation, University of Agricultural Sciences, Bangalore, India. Mani, M., 1989. A review of the pink mealybug, Maconellicoccus hirsutus (Green). Insect Sci. Appl. 10, 157e167. Mani, M., Thontadarya, T.S., 1989. Field evaluation of Cryptolaemus montrouzieri Muls. in the suppression of Maconellicoccus hirsutus Green on grapevine. J. Biol. Control 2, 14e16. Manjunath, T.M., 1985. India-Maconellicoccus hirsutus on grapevine. FAO Plant Prot. Bull. 33, 74. Meyerdirk, D.E., Warkentin, R., Attavian, B., Gersabeck, E., Francis, A., Adams, M., Francis, G., 1998. Biological Control of the Pink Hibiscus Mealybug Project Manual. United States Department of Agriculture, Washington, DC. Moffitt, M.J., 1999. Economic Risks to United States Agriculture of Pink Hibiscus Mealybug Invasion. University of Massachusetts, Amherst, MA. Muralidharan, C.M., Badaya, S.N., 2000. Mealy bug (Maconellicoccus hirsutus) outbreak on herbaceum cotton (Gossypium herbaceum) in Wagad cotton belt of Kachch. Ind. J. Agri. Sci. 70, 705e706. Patel, I.S., Dodia, D.A., Patel, S.N., 1990. First record of Maconellicoccus hirsutus as a pest of pigeonpea (Cajanus cajan). Indian J. Agri. Sci. 60, 645.
Patil, S.V., Salunke, B.K., Patil, C.D., Salunkhe, R.B., Gavit, P., Maheshwari, V.L., 2010. Potential of extracts of the tropical plant Balanites aegyptiaca (L) Del. (Balanitaceae) to control the mealybug, Maconellicoccus hirsutus (Homoptera: Pseudococcidae). Crop Prot. 29, 1293e1296. Persad, A., Khan, A., 2002. Comparison of life table parameters for Maconellicoccus hirsutus, Anagyrus kamali, Cryptolaemus montrouzieri and Scymnus coccivora. BioControl 47, 137e149. Persad, A., Khan, A., 2007. Effects of four host plants on biological Parameters of Maconellicoccus hirsutus green (homoptera: pseudococcidae) and efficacy of Anagyrus kamali moursi (Hymenoptera: Encyrtidae). J. Plant Prot. Res. 47 (1), 35e42. Pilkington, L.J., Hoddle, M.S., 2007. Use of life tables to quantify reproductive and developmental biology of Gonatocerus triguttatus (Hymenoptera: Mymaridae), an egg parasitoid of Homalodisca vitripennis (Hemiptera: Cicadellidae). Biol. Control 42, 1e8. Raju, A.K., Rao, P.R.M., Apparao, R.V., Readdy, A.S., Rao, K.K.P., 1988. Note on estimation of losses in yield of mesta due to mealy bug, Maconellicoccus hirsutus. Jute Develop. J. 8, 34e35. Serrano, M.S., Lapointe, S.L., 2002. Evaluation of host plants and a meridic diet for rearing Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) and its parasitoid Anagyrus kamali (Hymenoptera: Encyrtidae). Fla. Entomol. 85, 417e425. Singh, P., Ashby, M.D., 1985. Insect rearing management. In: Singh, P., Moore, R.F. (Eds.), Handbook of Insect Rearing, vol. I. Elsevier, Amsterdam, pp. 185e215. Tanwar, R.K., Jeyakumar, P., Monga, D., 2007. Mealybugs and their Management Tech. Bull. 19, September, 2007. Walton, V.M., Pringle, K.L., 2002. Evaluating effectiveness of mass releases of the vine mealybug (Planococcus ficus) parasitoid Coccidoxenoides peregrinus in Western Cape Province vineyards, South Africa. In: 1st International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, 14e16 July, 2002, pp. 524e532. Williams, D.J., 1985. Australian Mealy Bugs. British Museum (Natural History), London, United Kingdom. Yamamura, K., Kiritani, K., 1998. A simple method to estimate the potential increase in the number of generations under global warming in temperate zones. Appl. Entomol. Zool. 33, 289e298. Yang, P.J., Carey, J.R., Dowell, R.V., 1994. Temperature influences on the development and demography of Bactrocera doralis (Diptera: Tephritidae) in China. Environ. Entomol. 23, 971e974.
Contents lists available at SciVerse ScienceDirect
Crop Protection journal homepage: www.elsevier.com/locate/cropro
Studies on life cycle of mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), on different hosts at different constant temperatures Satish V. Patila, b, *, Chandrashekhar D. Patila, Rahul B. Salunkhea, Vijay L. Maheshwaria, Bipinchandra K. Salunkea a b
School of Life Sciences, North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India North Maharashtra Microbial Culture Collection Centre (NMCC), North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 May 2011 Received in revised form 12 August 2011 Accepted 16 August 2011
The life cycle of a laboratory reared parthenogenic line of mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) was investigated on six host plants (Lagenaria siceraria var.clavata, Solanum tuberosum L. var. Kufri Chandramukhi, Praecitrullus fistulosus (Stocks) Pangalo var. MTNH1, Cucurbita pepo var. Styriaca, Triticum aestivum L. var. Lokvan, H. rosa sinensis L.) at five constant temperatures (25, 29, 35, 38, 42 C). The number of emerging crawlers and adults as well as weight of adults varied with host and temperature. P. fistulosus and H. rosa sinensis were suitable hosts for laboratory rearing of M. hirsutus. However, ease of maintenance of P. fistulosus to produce M. hirsutus under laboratory conditions is an additional advantage compared to using green plants such as H. rosa sinensis. Among the range of constant temperatures, 38 C was found to be the most favourable for the development and survival of M. hirsutus. These results suggest that P. fistulosus fruits are suitable hosts for laboratory rearing and life cycle studies of M. hirsutus. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Laboratory rearing Longevity Praecitrullus fistulosus Hibiscus rosa-sinensis Crawler
1. Introduction Mealybugs (Hemiptera: Pseudococcidae) are plant sap-sucking insects that constitute a family with about 2000 species, some of which are major pests of agricultural plants (Williams, 1985; Gullan and Kosztarab, 1997). The pink hibiscus mealybug, Maconellicoccus hirsutus (Green) was first described as Phenacoccus hirsutus Green based on specimens collected in India on an undetermined shrub (Green, 1908). Ezzat (1958) re-described the species as M. hirsutus. The species is native to southern Asia, and has spread to other parts of the world such as Africa, and more recently North America and the Caribbean, where the range is still extending (Kairo et al., 2000). It attacks more than 200 plants, trees and shrubs with host records extending to 76 families, with some preference for Fabaceae, Malvaceae and Moraceae (Mani, 1989; Garland, 1998). M. hirsutus has been recorded causing economic damage to many crops including avocado, Persea americana Mill, cotton, Gosspium hirsutum L., peanut, Arachis hypogaea L., nursery crops, soya bean, Glycine max (L.) Merrill, and vegetables (Moffitt, 1999). The annual cost of control and * Corresponding author. School of Life Sciences, North Maharashtra University, Post Box 80, Jalgaon 425001, Maharashtra, India. Fax: þ91 257 2258403. E-mail addresses: [email protected] (S.V. Patil), bipin_salunke@yahoo. com (B.K. Salunke). 0261-2194/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.08.010
damages from invasion of M. hirsutus into US agriculture has been estimated at $750 million per year in the absence of control measures, with the global total being $5 billion (Moffitt, 1999; ARS, 2003). In India, losses have been reported for cotton (Muralidharan and Badaya, 2000), the fibre crops roselle, Hibiscus sabdariffa L., Kenaf, Hibiscus cannabinus L., and Boehmeria nivea L. (Ghose, 1972; Raju et al., 1988), grapevine, Vitis vinifera L. (Manjunath, 1985), pigeonpea, Cajanus cajan L. Millsp. (Patel et al., 1990), and Zizyphus mauritiana Lamarck (Balikai and Bagali, 2000). Despite the economic importance of M. hirsutus, there is a lack of detailed life history data on the species. Life tables and developmental rates are essential tools for investigating and understanding the impact of temperature on growth, survival, reproduction and rate of increase of an insect population. Life tables are especially important in understanding age dynamics of adult populations studied under controlled laboratory conditions (Carey, 2001) and in tackling the issue of life expectancy when affected by environmental changes (Pilkington and Hoddle, 2007). Biological control of mealybugs by laboratory rearing and releases of natural enemies in the field has been successful against a number of pseudococcid pests (Walton and Pringle, 2002). For rearing natural enemies of mealybugs such as the predatory beetles Cryptolaemus montrouzieri Mulsant and Schymnus coccivora Ramkrishna (Coleoptera: Coccinellidae), and the parasitoid, Anagyrus
1554
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
kamali Moursi (Hymenoptera: Encyrtidae) (Cross and Noyes, 1998), food plants and fruits that lead to high population growth rates of mealybugs need to be identified and exploited for laboratory rearing and production of biocontrol agents. However, there is not enough documented evidence about host suitability for rearing of M. hirsutus and its natural enemies (Johnson, 2010). Earlier reports on the life history of M. hirsutus were conducted at either a single constant temperature (Persad and Khan, 2002; Serrano and Lapointe, 2002) or fluctuating temperature regimens (Babu and Azam, 1987). Temperature is known to affect multiple biological traits such as sex ratio, adult life-span, survival, fecundity and fertility of insects including Bactrocera doralis Hendel, Clavigralla tomentosicollis Stål and Clavigralla shadabi Dolling (Singh and Ashby, 1985; Yang et al., 1994; Dreyer and Baumgartner, 1996). At low temperature, development occurs at a slower rate than at high temperature (Jarosik et al., 2004). It has been estimated that with a 2 C temperature increase insects might experience one to five additional life cycles per season (Yamamura and Kiritani, 1998). In this study, we examine the effects of different hosts and five constant temperatures (25e42 C) on the development of M. hirsutus. 2. Materials and methods A colony of M. hirsutus was initiated in February 2009 with adult females collected from an infested cotton field in the Jalgaon region of Maharashtra state, India. Samples were examined under a binocular dissection microscope in the laboratory. The life stages of M. hirsutus were identified using Hall (1926) and Meyerdirk et al. (1998). The colony of M. hirsutus was reared on Praecitrullus fistulosus (Stocks) Pangalo, as described by Patil et al. (2010). The colony was maintained by releasing one female per P. fistulosus fruit kept in glass trays (25 15 cm) at 30 2 C, 70 5% RH, and 16:8 h light: dark photoperiod. The fruits [Lagenaria siceraria (Mol.) Standley var.clavata (dudhi), Solanum tuberosum L. (sprouted potato) var. Kufri Chandramukhi, P. fistulosus (Stocks) Pangalo var. MTNH1 (tinda), Cucurbita pepo var. Styriaca (pumpkin)] were obtained from a supermarket, washed in tap water to ensure the removal of pesticide residues, dried and checked for prior infestation with insects. The fruits were kept in glass trays. Hibiscus rosa-sinensis L. obtained from a local nursery and 28 day old laboratory grown wheat, Triticum aestivum L. var. Lokvan, were used as the host plants for M. hirsutus. One gravid female per fruit in tray or per seedling in pot was released at 37.0 1.0 C and 70 5% relative humidity in an environmental chamber (REMI instruments, CHM 12S, India). The experiment continued until the death of the adult female on the host. Life cycle at each treatment was monitored by recording the
number of eggs, crawlers and adults using a stereomicroscope. The average weight of ten adult insects per fruit or seedling was recorded using an electronic balance (Shimadzu, LIBROR, AEG-120, Japan). The influence of five constant temperatures 25, 29, 35, 38, and 42 1.0 C at 70 5% relative humidity was examined on the cumulative growth of M. hirsutus in an environmental chamber (REMI instruments, CHM 12S, India). One gravid female was released per P. fistulosus in tray. The experiment continued until the death of the adult female on the host. Life cycle at each treatment was monitored by recording the number of eggs, crawlers, adults and the weight. Every experiment had three replicates of a fruit per tray or seedling per pot. The data were analysed by one way analysis of variance (ANOVA) using statistical software Minitab for Windows version 13. Treatment means were separated by Tukey’s multiple comparison test at a ¼ 0.05. 3. Results Hibiscus rosa sinensis was found to be the most suitable host (Table 1) with the highest number of eggs, crawlers and adults along with greater longevity (time from egg hatch to death of adult). Fruits of P. fistulosus were found to be the second most suitable host after H. rosa sinensis. Hosts C. pepo (93%), L. siceraria (73%), S. tuberosum (33%) and T. aestivum (29%) had fewer eggs as compared to P. fistulosus, thus resulting in reduced subsequent cumulative survival. The longevity of adult females was similar when reared on P. fistulosus, C. pepo and H. rosa sinensis, at close to 21 days. Female longevity was significantly shorter by 8.7 days on T. aestivum, 6.3 days on S. tuberosum and 2.3 days on L. siceraria compared to P. fistulosus (Table 1). Females reared on C. pepo, H. rosa sinensis and P. fistulosus produced significantly more eggs than females reared on other hosts (Table 1). However, the number of eggs obtained on sprouted potato and wheat were 67 and 71% fewer, respectively, than on P. fistulosus. The mean percentage of adult emergence from laid eggs was found to be highest for females reared on P. fistulosus (41.2%) and H. rosa sinensis (41.5%). Moderate adult emergence was obtained for females reared on C. pepo (30.0%) and L. siceraria (28.5%), whereas the lowest adult emergence was observed for S. tuberosum (20.6%), followed by T. aestivum (11.3%). Females reared at 25 C and 42 C produced significantly fewer eggs and reduced numbers of crawlers, adults, adult weight and longevity (Table 2). The egg production, number of crawlers and adult formation increased with temperature until 38 C. The developmental time also decreased with an increase in temperature from 25 to 42 C.
Table 1 Life cycle of the mealybug, Maconellicoccus hirsutus on different hosts.a Hosts
Number of eggs
Number of crawlers
Dudhi (Lagenaria siceraria var.clavata) Sprouted potato (Solanum tuberosum L. var. Kufri Chandramukhi) Tinda (Praecitrullus fistulosus(Stocks) Pangalo var. MTNH1) Pumpkin (Cucurbita pepo var. Styriaca) Wheat plant (Triticum aestivum L. var. Lokvan) Hibiscus plant (H. rosa sinensis L.) F df P
202.00 (1.00) d 92.33 (1.53) e
161.33 (2.08) d 55.33 (1.53) e
57.67 (1.53) d 19.00 (2.00) e
18.67 (0.58) b 14.67 (0.58) c
278.33 (1.53) b
225.00 (2.00) b
114.67 (2.08) b
21.00 (1.00) a
258.67 (1.15) c 79.67 (1.53) f 302.00 (1.00) a 16036.24 5, 12 <0.0001
216.00 (3.61) c 38.67 (4.51) f 268.33 (2.08) a 3334.75 5, 12 <0.0001
77.67 (1.53) c 9.00 (1.00) f 125.33 (1.53) a 2544.28 5, 12 <0.0001
21.00 (1.00) a 12.33 (0.58) d 21.00 (1.00) a 63.53 5, 12 <0.0001
Data are presented as mean (SD). Means within a given column followed by the same letter are not significantly different, Tukey’s MRT, (a ¼ 0.05). a One female was released on each host.
Number of Adults
Time (Days)
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
1555
Table 2 Effect of different constant temperatures on the life cycle of the mealybug, Maconellicoccus hirsutus.a Treatment ( C)
Number of eggs
Number of crawlers
Number of adults
Weight of adults (mg)
Longevity (Days)
25 29 35 38 42 F df P
74.00 (1.00) 155.33 (1.53) 222.33 (1.53) 272.67 (1.53) 76.00 (2.00) 9704.06 4, 10 <0.0001
55.33 (1.53) 132.67 (1.15) 181.67 (1.53) 246.00 (1.00) 43.00 (1.00) 13716.40 4, 10 <0.0001
12.00 (1.00) 35.67 (1.53) 85.67 (1.53) 112.33 (1.53) 16.00 (1.00) 3306.57 4, 10 <0.0001
3.87 (0.12) 4.00 (0.10) 5.30 (0.10) 5.67 (0.12) 3.73 (0.06) 242.93 4, 10 <0.0001
22.33 (0.58) 20.33 (1.15) 19.33 (0.58) 19.33 (0.58) 18.00 (0.00) 16.64 4, 10 <0.0001
d c b a d
d c b a e
e c b a d
c c b a c
a b bc bc c
Data are presented as mean (SD). Means within a given column followed by the same letter are not significantly different, Tukey’s MRT, (a ¼ 0.05). a One female was released on each Praecitrullus fistulosus.
4. Discussion P. fistulosus fruits are reported here for the first time for laboratory rearing of M. hirsutus. This host produced a large number of insects with the same developmental rate and a high survival rate when compared to previously used hosts such as C. pepo, S. tuberosum and Cucurbita moschata (Duchesne) cv. Chirimen (Serrano and Lapointe, 2002). H. rosa sinensis is a host plant frequently found with natural infestations of M. hirsutus (Persad and Khan, 2007; Tanwar et al., 2007). Wheat has been reported as an incidental host on which crawlers were able to establish and produce injury symptoms (Dhawan, 2007). Our study showed that M. hirsutus could complete their life cycle and reproduce on wheat in the laboratory. However, the weak performance of M. hirsutus on wheat reduces its suitability as a host for laboratory rearing. The difference in fecundity of M. hirsutus on different host plant species or food substrates is supported by earlier reports where Serrano and Lapointe (2002) obtained the highest mean fecundity when the females were reared on Japanese pumpkin (C. moschata) (162 eggs) and the lowest on a meridic diet (59 eggs). Other reports of M. hirsutus fecundity varied greatly from 84 to 654 eggs on Hibiscus sabdariffa L. as reported by Ghose (1972) and 386e540 eggs on V. vinifera L. as reported by Mani (1986). Most of the previous studies are from countries where average field temperatures are below 30 C. In the present study area (Jalgaon, 21 050 N 75 400 E, Elevation 218 masl), there are two distinct seasons, NovembereMarch (winter - average temperature 7e25 C) and AprileOctober (summer - average temperature 23e45 C). The temperatures in our study are within the average field conditions in India. Seasonal climatic patterns influence mealybug populations. In the field, we observed that mealybug infestation increased with temperature. This prompted us to study the effect of a range of temperatures on the life cycle performance of mealybugs in a laboratory setting. Research reports from the Caribbean (Kairo et al., 2000), South India (Mani and Thontadarya, 1989) and Australia (Goolsby et al., 2002) showed that populations were low during the rainy season and winter, and peaked during the summer months. In the present study, we also found that increased temperature accelerated the development of female M. hirsutus. Previous reports by other researchers also reported an increased developmental rate with temperature up to 27 C (Serrano and Lapointe, 2002; Babu and Azam, 1987). At lower temperatures, reduced development would be expected primarily because the immature stages convert less food into body tissue, resulting in low growth and thus longer developmental times (Atkinson and Sibly, 1997). In contrast, Chong et al. (2008) reported production of 260e300 eggs by M. hirsutus reared on hibiscus plant cuttings at 20e27 C, but only 100 eggs at 30 C and occurrence of complete development in 29 days at 27 C. An ideal host for the rearing of M. hirsutus should produce adults within a short development time. Females should be able to produce
large ovisacs with a high survival rate of offspring. P. fistulosus fruits have the added advantage of being convenient for the application of insecticidal test materials to carry out bioefficacy assays (Patil et al., 2010), and are easy to handle for the measurement of the number of eggs, crawlers and adults. P. fistulosus fruits are an easily available, cheap source of host material for rearing of mealybugs. In this study, we demonstrated that the most suitable rearing temperature for M. hirsutus was 38 C. The investigations can be exploited for laboratory rearing and production of biocontrol agents of mealybugs such as predatory beetles and the parasitoids at different temperature range in diverse areas. In addition to this, the study can help to determine the conditions in the field that maximize the efficacy of biocontrol agents of mealybugs. Similarly, different strains of pest and natural enemies need to be studied from areas with varying environmental conditions.
Acknowledgement Financial assistance from the Department of Biotechnology, New Delhi, in the form of a project grant (2010e2013) is gratefully acknowledged [BT/PR 12694/AGR/05/474/(letter I)].
References ARS, 2003. On the Lookout for Scaly Invaders. URL. http://www.ars.usda.gov/is/AR/ archive/dec03/scaley1203.pdf. Atkinson, D., Sibly, R.M., 1997. Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol. Evol. 6, 235e239. Babu, T.R., Azam, K.M., 1987. Studies on biology, host spectrum and seasonal population fluctuation of the mealybug, Maconellicoccus hirsutus Green on grapevine. Indian J. Hortic. 44, 284e288. Balikai, R.A., Bagali, A.N., 2000. Population density of mealy bug, Maconellicoccus hirsutus on ber (Zizyphus mauritiana) and economic losses. Agri. Sci. Dig. 20, 62e63. Carey, J.R., 2001. Insect biodemography. Annu. Rev. Entomol. 46, 79e110. Chong, J.H., Amy, L.R., Catharinem, M.M., 2008. Life history of the mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), at constant temperatures. Environ. Entomol. 37, 323e332. Cross, A.E., Noyes, J.S., 1998. Dossier on Anagyrus kamali Moursi an Exotic Natural Enemy for Biological Control of the Hibiscus Mealybug in the Caribbean. International Institute of Biological Control, Trinidad and Tobago, 26 pp. Dhawan, A.K., 2007. Status of Mealy Bug in Punjab. URL. http://www.ncipm.org.in/ MealybugPunjab.doc. Dreyer, H., Baumgartner, J., 1996. Temperature influence on cohort parameters and demographic characteristics of the cowpea coreids Clavigralla tomentosicollis and C. shadabi. Entomol. Exp. Appl. 78, 201e213. Ezzat, Y.M., 1958. Maconellicoccus hirsutus (Green), a new genus, with redescription of the species [Homoptera: Pseudococcidae-Coccoidea]. Bull. Entomol. Soc. Egypt. 42, 377e383. Garland, J.A., 1998. Pest Risk Assessment of the Pink Mealy Bug Maconellicoccus hirsutus (Green), with particular reference to Canadian Greenhouses. PRA 96e21. Canadian Food Inspection Agency, Ottawa (CA). Ghose, S.K., 1972. Biology of the mealybug, Maconellicoccus hirsutus Green (Pseudococcidae: Hemiptera). Indian Agric. 16, 323e332. Goolsby, J.A., Kirk, A.A., Meyerdirk, D.E., 2002. Seasonal abundance and natural enemies of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Australia. Fla. Entomol. 85, 494e498.
1556
S.V. Patil et al. / Crop Protection 30 (2011) 1553e1556
Green, E.E., 1908. Remarks on Indian scale insects (Coccidae), Part III. With a catalogue of all species hitherto recorded from the Indian continent. Mem. Dep. Agric. India Ent. Ser. 2, 15e46. Gullan, P.J., Kosztarab, M., 1997. Adaptations in scale insects. Annu. Rev. Entomol. 42, 23e50. Hall, W.J., 1926. The Hibiscus mealybug (Phenacoccus hirsutus, Green) in Egypt in 1925 with notes on the introduction of Cryptolaemus montrouzieri, Muls. Ministry of Agriculture, Egypt. Tech. Scientific Serv. Bull. No. 70, 1e15. Jarosik, V., Kratochvil, L., Honek, A., Dixon, A.F.G., 2004. A general rule for the dependence of developmental rate in ectothermic animals. Proc. R. Soc. B 271 (Suppl.), S219eS221. Johnson, T., 2010. Biology of the Oleander mealybug, Paracoccus burnerae (brain) (hemiptera: pseudococcidae). M.Sc. Thesis, University of Stellenbosch, South Africa. Kairo, M.T.K., Pollard, G.V., Peterkin, D.D., Lopez, V.F., 2000. Biological control of the hibiscus mealy bug, Maconellicoccus hirsutus in the Caribbean. Int. Pest Manag. 5, 241e254. Mani, M., 1986. Distribution, bioecology and management of the grape mealybug (Maconellicoccus hirsutus Green) with special reference to its natural enemies. PhD dissertation, University of Agricultural Sciences, Bangalore, India. Mani, M., 1989. A review of the pink mealybug, Maconellicoccus hirsutus (Green). Insect Sci. Appl. 10, 157e167. Mani, M., Thontadarya, T.S., 1989. Field evaluation of Cryptolaemus montrouzieri Muls. in the suppression of Maconellicoccus hirsutus Green on grapevine. J. Biol. Control 2, 14e16. Manjunath, T.M., 1985. India-Maconellicoccus hirsutus on grapevine. FAO Plant Prot. Bull. 33, 74. Meyerdirk, D.E., Warkentin, R., Attavian, B., Gersabeck, E., Francis, A., Adams, M., Francis, G., 1998. Biological Control of the Pink Hibiscus Mealybug Project Manual. United States Department of Agriculture, Washington, DC. Moffitt, M.J., 1999. Economic Risks to United States Agriculture of Pink Hibiscus Mealybug Invasion. University of Massachusetts, Amherst, MA. Muralidharan, C.M., Badaya, S.N., 2000. Mealy bug (Maconellicoccus hirsutus) outbreak on herbaceum cotton (Gossypium herbaceum) in Wagad cotton belt of Kachch. Ind. J. Agri. Sci. 70, 705e706. Patel, I.S., Dodia, D.A., Patel, S.N., 1990. First record of Maconellicoccus hirsutus as a pest of pigeonpea (Cajanus cajan). Indian J. Agri. Sci. 60, 645.
Patil, S.V., Salunke, B.K., Patil, C.D., Salunkhe, R.B., Gavit, P., Maheshwari, V.L., 2010. Potential of extracts of the tropical plant Balanites aegyptiaca (L) Del. (Balanitaceae) to control the mealybug, Maconellicoccus hirsutus (Homoptera: Pseudococcidae). Crop Prot. 29, 1293e1296. Persad, A., Khan, A., 2002. Comparison of life table parameters for Maconellicoccus hirsutus, Anagyrus kamali, Cryptolaemus montrouzieri and Scymnus coccivora. BioControl 47, 137e149. Persad, A., Khan, A., 2007. Effects of four host plants on biological Parameters of Maconellicoccus hirsutus green (homoptera: pseudococcidae) and efficacy of Anagyrus kamali moursi (Hymenoptera: Encyrtidae). J. Plant Prot. Res. 47 (1), 35e42. Pilkington, L.J., Hoddle, M.S., 2007. Use of life tables to quantify reproductive and developmental biology of Gonatocerus triguttatus (Hymenoptera: Mymaridae), an egg parasitoid of Homalodisca vitripennis (Hemiptera: Cicadellidae). Biol. Control 42, 1e8. Raju, A.K., Rao, P.R.M., Apparao, R.V., Readdy, A.S., Rao, K.K.P., 1988. Note on estimation of losses in yield of mesta due to mealy bug, Maconellicoccus hirsutus. Jute Develop. J. 8, 34e35. Serrano, M.S., Lapointe, S.L., 2002. Evaluation of host plants and a meridic diet for rearing Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) and its parasitoid Anagyrus kamali (Hymenoptera: Encyrtidae). Fla. Entomol. 85, 417e425. Singh, P., Ashby, M.D., 1985. Insect rearing management. In: Singh, P., Moore, R.F. (Eds.), Handbook of Insect Rearing, vol. I. Elsevier, Amsterdam, pp. 185e215. Tanwar, R.K., Jeyakumar, P., Monga, D., 2007. Mealybugs and their Management Tech. Bull. 19, September, 2007. Walton, V.M., Pringle, K.L., 2002. Evaluating effectiveness of mass releases of the vine mealybug (Planococcus ficus) parasitoid Coccidoxenoides peregrinus in Western Cape Province vineyards, South Africa. In: 1st International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, 14e16 July, 2002, pp. 524e532. Williams, D.J., 1985. Australian Mealy Bugs. British Museum (Natural History), London, United Kingdom. Yamamura, K., Kiritani, K., 1998. A simple method to estimate the potential increase in the number of generations under global warming in temperate zones. Appl. Entomol. Zool. 33, 289e298. Yang, P.J., Carey, J.R., Dowell, R.V., 1994. Temperature influences on the development and demography of Bactrocera doralis (Diptera: Tephritidae) in China. Environ. Entomol. 23, 971e974.