Abstract
Aenasius arizonensis (Girault) (Hymenoptera: Encyrtidae) is an important solitary endoparasitoid of mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). Studies on seasonal and biological interactions between host and parasitoid are important to optimize the mass production and field release of high-quality females. We investigated the influence of different crop seasons viz., pre-monsoon, monsoon and post-monsoon and host stages viz., three nymphal instars (1st, 2nd and 3rd) and adult stage of P. solenopsis on the development, longevity, fecundity and sex ratio of its parasitoid, A. arizonensis. A. arizonensis female parasitized all life stages of its host except the 1st instar nymphs. Only males emerged from parasitized 2nd instar nymphs, while the sex ratio in the later host instars was strongly female-biased. The adult host stage was most suitable for A. arizonensis in terms of shorter development time, while the 3rd instar nymphal stage was most suitable with respect to higher fecundity, proportion of adults emerged and more females in the progeny. Among different seasons, post-monsoon season (September–October) with temperature (25 to 29 °C) and relative humidity (68 to 73%) was most suitable for the overall fitness of the parasitoid. The findings of this study have implications in designing mass rearing of this parasitoid and devising an effective biological control strategy for P. solenopsis on cotton.
Similar content being viewed by others
References
Abdin, Z., Arif, M. J., Gogi, M. D., Arshad, M., Hussain, F., Abbas, S. K., Shaina, H., & Manzoor, A. (2012). Biological characteristics and host stage preference of mealybug parasitoid Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae). Pakistan Entomologist, 34, 47–50.
Abdin, Z., Hussain, F., Khan, M. A., Abbas, S. K., Manoor, A., & Shaina, H. (2013). Reproductive fitness of mealybug parasitoid, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae). World Applied Sciences Journal, 26, 1198–1203.
Anonymous. (2015). Package of practices for Kharif crops (pp. 41–65). Ludhiana: Punjab Agricultural University.
Babendreier, D. (2007). Life history of Aptesis nigrocincta (Hymenoptera: Ichneumonidae) a cocoon parasitoid of the apple sawfly, Hoplocampa testudinea (Hymenoptera: Tenthredinidae). Bulletin of Entomological Research, 90, 291–297.
Badshah, H., Ullah, F., Calatayud, P. A., & Crickmore, N. (2016). Host stage preference and parasitism behaviour of Aenasius bambawalei an encyrtid parasitoid of Phenacoccus solenopsis. Biocontrol Science and Technology, 26, 1605–1616.
Bertschy, C., Turlings, T. C. J., Bellotti, A., & Dorn, S. (2000). Host stage preference and sex allocation in Aenasius vexans, an encyrtid parasitoid of the cassava mealybug. Entomologia Experimentalis et Applicata, 95, 283–291.
Charnov, E. L. (1982). The theory of sex allocation. Princeton: Princeton University Press.
Charnov, E. L., Los-den Hartogh, R. L., Jones, W. T., & Van den Assem, J. (1981). Sex ratio evolution in a variable environment. Nature, 289, 27–33.
Chen, H. Y., Run-Xin, C. A. O., & Zai-Fu, X. U. (2010). First record of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), a parasitoid of the mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) from China. Journal of Environmental Entomology, 32, 280–282.
Chong, J. H., & Oetting, R. D. (2006). Host stage selection of the mealybug parasitoid. Anagyrus sp.nov.nr.sinope. Entomologia Experimentalis et Applicata, 121, 39–50.
Colinet, H., Salin, C., Boivin, G., & Hance, T. H. (2005). Host age and fitness related traits in koinobiont aphid parasitoid. Environmental Entomology, 30, 473–479.
Crawley, M. J. (1993). GLIM for ecologists. Oxford: Blackwell Scientific Publications.
Fallahzadeh, M., Abdimaleki, R., & Saghaei, N. (2014). New records of Tetracneminae (Hymenoptera, Chalcidoidea, Encyrtidae) from Iran. Turkish Journal of Zoology, 38, 515–518.
Fand, B. B., Gautam, R. D., & Suroshe, S. S. (2011). Suitability of various stages of mealybug, Phenacoccus solenopsis (Homoptera: Pseudococcidae) for development and survival of the solitary endoparasitoid, Aenasius bambawalei (Hymenoptera: Encyrtidae). Biocontrol Science and Technology, 21, 51–55.
Fuchs, T. W., Stewart, J. W., Minzenmayer, R., & Rose, M. (1991). First record of Phenacoccus solenopsis Tinsley in cultivated cotton in the United States. Southwestern Entomologist, 16, 215–221.
García Morales, M., Denno, B.D., Miller, D.R., Miller, G.L., Ben-Dov, Y. & Hardy, N.B. (2016). ScaleNet: A literature–based model of scale insect biology and systematic. Database https://doi.org/10.1093/database/bav118. Available at http://scalenet.info .
Godfray, H. C. J. (1994). Parasitoids: Behavioral and evolutionary ecology. Princeton: Princeton University Press.
Gulec, G., Kilincer, A. N., Kaydan, M. B., & Ulgenturk, S. (2007). Some biological interactions between the parasitoid Anagyrus pseudococci (Girault) (Hymenoptera : Encrytidae) and its host Planococcus ficus (Signoret) (Hemiptera: Coccidae: Pseudococcidae). Journal of Pest Science, 80, 43–49.
Hagvar, E. B., & Hofsvang, T. (1991). Aphid parasitoids (Hymenoptera: Aphidiidae): Biology, host selection, and use in biological control. Biocontrol News Information, 12, 3–41.
Hardy, I. C. W. (1992). Non-binomial sex allocation and brood sex ratio variances in the parasitoid Hymenoptera. Oikos, 65, 143–150.
Hardy, I. C. W., Dijkstra, L. J., Gillis, J. E. M., & Luft, P. A. (1998). Patterns of sex ratio, virginity and developmental mortality in gregarious parasitoids. Biological Journal of the Linnean Society, 64, 239–270.
Harvey, J. A. (2005). Factors affecting the evolution of development strategies in parasitoid wasps: The importance of functional constraints and incorporating complexity. Entomologia Experimentalis et Applicata, 117, 1–13.
Harvey, J. A., Harvey, I. F., & Thompson, D. J. (1994). Flexible larval growth allows use of a range of host sizes by a parasitoid wasp. Ecology, 75, 1420–1428.
Hayat, M. (2009). Description of a new species of Aenasius Walker (Hymenoptera: Encyrtidae), India. Biosystematica, 3, 21–26.
He, L. F., Feng, D. D., Li, P., Zhou, Z. S., & Xu, Z. F. (2015). Reproductive modes and daily fecundity of Aenasius bambawalei (Hymenoptera: Encyrtidae), a parasitoid of Phenacoccus solenopsis (Hemiptera: Pseudococcidae). Florida Entomologist, 98, 358–360.
He, L. F., Li, P., Zhou, Z. S., & Xu, Z. F. (2018). Temperature-dependent parasitism and development in Aenasius arizonensis Girault (Hymenoptera: Encyrtidae), a solitary endoparasitoid of Phenacoccus solenopsis (Hemiptera:Pseudococcidae). International Journal of Pest Management, 64, 45–50.
Hochberg, Y. (1988). A sharper Bonferroni procedure for multivariate tests of significance. Biometrika, 75, 800–802.
Hu, J.S., Gelman, D.B. & Blackburn, M.B. (2003). Age specific interaction between the parasitoid, Encarsia formosa and its host the silverleaf whitefly Bemisia tabaci (strain B) Journal of Insect Science 3: 1–10.
Iqbal, M. S., Abdin, Z., Arshad, M., Abbas, S. K., Tahir, M., Jamil, A., & Manzoor, A. (2016). The role of parasitoid age on the fecundity and sex ratio of the parasitoid, Aenasius bambawalei (Hayat) (Hymenoptera: Encyrtidae). Pakistan Journal of Zoology, 48, 67–−72.
Jervis, M. A., & Copland, M. J. W. (1996). The life cycle. In M. Jervis & N. Kidd (Eds.), Insect natural enemies: Practical approaches to their study and evaluation (pp. 63–161). London: Chapman & Hall.
Jervis, M. A., Ellers, J., & Harvey, J. A. (2008). Resource acquisition, allocation and utilization in parasitoid reproductive strategies. Annual Review of Entomology, 53, 361–385.
Jong De, P. W., & van Alphen, J. J. M. (1989). Host stage selection and sex allocation in Leptomastix dactylopii, a parasitoid of Planococcus citri. Entomologia Experimentalis et Applicata, 50, 161–169.
Kant, R., Minor, M. A., & Trewick, S. A. (2012). Fitness gain in a koinobiont parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) by parasitising hosts of different ages. Journal of Asia Pacific Entomology., 15, 83–87.
Karamaouna, F., & Copland, M. J. W. (2000). Host suitability, quality and host size preference of Leptomastix epona and Pseudaphycus flavidulus, two endoparasitoids of the mealybug, Pseudococcus viburni and host size effect on parasitoid sex ratio and clutch size. Entomologia Experimentalis et Applicata, 96, 149–158.
Khan, M., Quade, A., Byers, K., Hall, Z. & Grams, R. (2012). Record of Aenasius bambawalei Hayat, a parasitoid of solenopsis mealybug, in Australia. In: Proc 16th Australian Cotton Conference. Cotton Research and Development Corporation. Queensland, Australia.
Khuhro, S. N., Kalroo, M., & Mahmood, R. (2011). Present status of mealybug Phenacoccus solenopsis (Tinsley) on cotton and other plants in Sindh (Pakistan). CABI, 45, 268–271.
King, B.H. (1989). A test of local mate competition theory with a solitary species of parasitoid wasp, Spalangia cameroni. Oikos 55, 50–54.
King, B. H. (1993). Sex ratio manipulation by parasitoid wasps. In D. L. Wrench & M. A. Ebbert (Eds.), Evolution and diversity of sex ratio in insects and mites (pp. 418–441). New York: Chapman and Hall.
Lampson, L. J., Morse, J. G., & Luck, R. F. (1996). Host selection, sex allocation, and host feeding by Metaphycus helvolus (Hymenoptera: Encyrtidae) on Saissetia oleae (Homoptera: Coccidae) and its effect on parasitoid size, sex, and quality. Environmental Entomology, 25, 283–294.
Liu, S. S. (1985). Aspects of numerical and functional responses of the aphid parasite, Aphidius sonchi, in the laboratory. Entomologia Experimentalis et Applicata, 37, 247–256.
Liu, S., Wang, X., Shi, Z., & Gebremeskel, F. B. (2001). The biology of Diadromus collaris (Hymenoptera: Ichneumonidae), a pupal parasitoid of Plutella xylostella (Lepidoptera: Plutellidae), and its interactions with Oomyzus sokolowskii (Hymenoptera: Eulopidae). Bulletin of Entomological Research, 91, 461–469.
López, O. P., Henaut, Y., Cancino, J., Lambin, M., López, L. C., & Rojas, J. C. (2009). Is host size: An indicator of quality in the mass-reared parasitoid Diachasmimorpha Longicaudata (Hymenoptera: Braconidae)? Florida. Entomologist, 92, 441–449.
Mahmood, R. (2008). Breakthrough in biological control of mealybug in Pakistan. Biocontrol News Information., 29, 38–39.
Mohammad, J. K., Jassany, R. F. A., & Ali, A. S. A. (2015). Influence of temperature on some biological characteristics of Trichogramma evanescens (Westwood) (Hymenoptera: Trichogrammatidae) on the egg of lesser date moth Batrachedra amydraula Meyrick. Journal of Biological Control, 29, 125–130.
Nagrare, V., Kranthi, S., Biradar, V.K., Zade, N.N., Sangode, V., Kakde, G., Shukla, R.M., Shivare, D., Khadi, B.M. & Kranthi, K.R. (2009). Widespread infestation of the exotic mealybug species, Phenacoccus solenopsis (Tinsley) (Hemiptera: Pseudococcidae) on cotton in India. Bulletin of Entomological Research. 99, 537–541.
Nagrare, V., Kranthi, S., Kumar, R., Dhara Jothi, B., Amutha, M., Deshmukh, A., Bisane, K. & Kranthi, K. (2011). Compendium of Cotton Mealybugs. CICR, Shankar Nagar, Nagpur, India, pp 29.
Napoleon, M. E., & King, B. H. (1999). Offspring sex ratio response to host size in the parasitoid wasp Spalangia endius. Behavioral Ecology and Sociobiology, 46, 325–332.
Neveu, N., Krespi, L., Kacem, N., & Nenon, J. P. (2000). Host-stage selection by Trybliographa rapae, a parasitoid of the cabbage root fly Delia radicum. Entomologia Experimentalis et Applicata, 96, 231–237.
Noyes, J.S. & Hayat, M. (1994). Oriental mealybug parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). CAB International, Abingdon, UK.
Ode, P. J., & Hardy, I. C. W. (2008). Parasitoid sex ratios and biological control. In E. Wajnberg, C. Bernstein, & J. J. M. van Alphen (Eds.), Behavioural ecology of insect parasitoids: From theoretical approaches to field applications (pp. 253–−285). Oxford: Blackwell Publishing.
Poorani, J., Rajeshwari, S. K., & Gupta, A. (2009). Notes on diagnosis and biology of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), a parasitoid of the invasive mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Sternorrhyncha: Pseudococcidae). Journal of Biological Control, 23, 463–466.
Ram, P., & Saini, R. K. (2010). Biological control of solenopsis mealybug Phenacoccus solenopsis Tinsley on cotton: A typical example of fortuitous biological control. Journal of Biological Control, 24, 104–109.
Ram, P., Saini, R. K., & Vijaya. (2009). Preliminary studies on field parasitization and biology of solenopsis mealybug parasitoid, Aenasius bambawalei Hayat (Encyrtidae: Hymenoptera). Journal of Cotton Research Development, 23, 313–−315.
Sequeira, R., & Mackauer, M. (1992). Covariance of adult size and development time in the parasitoid wasp Aphidius ervi in relation size of its host, Acyrtosiphon pisum. Evolutionary Ecology, 6, 34–44.
Sequeira, R., & Mackauer, M. (1993). The nutritional ecology of parasitoid wasp, Ephedrus californicus baker (Hymenoptera: Aphidiidae). Canadian Entomologist, 125, 423–430.
Souissi, R., & Le Ru, B. (1997). Comparative life table statistics of Apoanagyrus lopezi reared on the cassava mealybug Phenacoccus manihoti fed on four host plants. Entomologia Experimentalis et Applicata, 36, 113–119.
Vijaya, & Ram, P. (2013). Effect of host stage on parasitization and biological characteristics of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), a parasitoid of Phenacoccus solenopsis Tinsley. Journal of Biological Control, 27, 126–−129.
Wang, Y., Watson, G. W., & Zhang, R. (2010). The potential distribution of an invasive mealybug Phenacoccus solenopsis and its threat to cotton in Asia. Agriculture and Forest Entomology, 12, 403–416.
West, S. A. (2009). Sex Allocation. Woodstock: Princeton University Press.
West, S. A., & Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295, 1685–1688.
Wilson, K., & Hardy, I. C. W. (2002). Statistical analysis of sex ratios: An introduction. In I. C. W. Hardy (Ed.), Sex Ratios: Concepts and Research Methods (pp. 48–92). Cambridge: Cambridge University Press.
Yamane, T., Goenaga, J., Rönn, J. L., & Arnqvist, G. (2015). Male seminal fluid substances affect sperm competition success and female reproductive behavior in a seed beetle. PLoS One. https://doi.org/10.1371/journal.pone.0123770.
Zhang, J., Jun, H., Yao-bin, L. U., & Xia, T. (2016). Effects of temperature and host stage on the parasitization rate and offspring sex ratio of Aenasius bambawalei Hayat in Phenacoccus solenopsis Tinsley. Peer J. https://doi.org/10.7717/peerj.1586.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Karmakar, P., Shera, P. Seasonal and biological interactions between the parasitoid, Aenasius arizonensis (Girault) and its host, Phenacoccus solenopsis Tinsley on cotton. Phytoparasitica 46, 661–670 (2018). https://doi.org/10.1007/s12600-018-0696-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12600-018-0696-0