INFLUENCE OF HOST STAGE ON OVIPOSITION, DEVELOPMENT, AND SEX RATIO OF Anagyrus lopezi (DE SANTIS) (HYMENOPTERA: ENCYRTIDAE), A PARASITOID OF THE CASSAVA MEALYBUG, Phenacoccus manihoti MATILE-FERRERO (HEMIPTERA: PSEUDOCOCCIDAE)

Authors

  • Evie Adriani Study Program of Agrotechnology, Faculty of Agriculture, Ichsan University of Gorontalo
  • Aunu Rauf Department of Plant Protection, Faculty of Agriculture, IPB University
  • Pudjianto Department of Plant Protection, Faculty of Agriculture, IPB University

DOI:

https://doi.org/10.23960/jhptt.220130-139

Keywords:

Anagyrus lopezi, cassava, mealybug, parasitoid, Phenacoccus manihoti

Abstract

Influence of host stage on oviposition, development, and sex ratio of Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae), a parasitoid of the cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). The parasitoid Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae) was introduced from Thailand into Indonesia in early 2014 to control the invasive cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). Because of the need to produce large numbers of high-quality females, research was conducted in the laboratory to determine host stage preference for A. lopezi on different instars of P. manihoti. Individual female wasps were exposed to first, second, third instar nymphs, and pre-reproductive adult mealybugs. In the no-choice test, the frequency of parasitized hosts and the number of eggs laid per host was significantly higher in second and third instar nymphs as well as adult mealybugs compared to first instar nymphs. In the two-choice test, third instars nymphs and adult mealybugs were the most preferred host for oviposition. Immature development of parasitoids was faster and the ratio of female to male parasitoids was higher following oviposition in second and third instar nymphs and pre-reproductive adult hosts, compared to the first instar nymphs. Our findings indicate that the use of pre-reproductive adults as hosts in a mass-rearing program would be the most productive and fastest way to produce A. lopezi populations with a female-biased sex ratio. Field release of parasitoids should be conducted when the host’s third instar nymph is the most abundant because the period during which preferred and suitable host stages are available would be the longest.

References

Abduchalek B, Rauf A, & Pudjianto. 2017. Kutu putih singkong, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae): persebaran geografi di Pulau Jawa dan rintisan pengendalian hayati. J. HPT Tropika. 17(1): 1–8.

Adriani E, Rauf A, & Pudjianto. 2016. Laju enkapsulasi parasitoid Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae) oleh kutu putih singkong Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). JEI. 13(3): 147–155.

Badshah H, Ullah F, Calatayud PA, & Crickmore N. 2016. Host stage preference and parasitism behaviour of Aenasius bambawalei an encyrtid parasitoid of Phenacoccus solenopsis. Biocontrol Sci. Technol. 26(12): 1605–1616.

Bellotti A, Campo BVH, & Hyman G. 2012. Cassava production and pest management: Present and potential threats in a changing environment. Trop. Plant Biol. 5(1): 39–72.

Bertschy C, Turlings TCJ, Bellotti A, & Dorn S. 2000. Host stage preference and sex allocation in Aenasius vexans, an encyrtid parasitoid of the cassava mealybug. Entomol. Exp. Appl. 95(3): 283–291.

Blumberg D. 1997. Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol. Control. 8(3): 225–236.

Cadée N & van Alphen JJM. 1997. Host selection and sex allocation in Leptomastidea abnormis, a parasitoid of the citrus mealybug Planococcus citri. Entomol. Exp. Appl. 83(3): 277–284.

Charnov EL, Los-den-Hartogh RL, Jones WT, & van den Assem J. 1981. Sex ratio evolution in a variable environment. Nature. 289(5793): 27–33.

Chong JH & Oetting RD. 2006. Host stage selection of the mealybug parasitoid Anagyrus spec. nov near sinope. Entomol. Exp. Appl. 121(1): 39–50.

Fanani MZ, Rauf A, Maryana N, Nurmansyah A, & Hindayana D. 2019. Geographic distribution of the invasive mealybug Phenacoccus manihoti and its introduced parasitoid Anagyrus lopezi in parts of Indonesia. Biodiversitas. 20(12): 3751–3757.

Fand BB, Gautam RD, & Suroshe SS. 2011. Suitability of various stages of mealybug, Phenacoccus solenopsis (Homoptera: Pseudococcidae) for development and survival of the solitary endoparasitoid, Aenasius bambawalei (Hymenoptera: Encyrtidae). Biocontrol Sci. Technol. 21(1): 51–55.

Godfray HCJ. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, New Jersey.

Graziosi I, Minato N, Alvarez E, Ngo DT, Hoat TX, Aye TM, Pardo JM, Wongtiem P, & Wyckhuys KAG. 2016. Emerging pests and diseases of South-east Asia cassava: a comprehensive evaluation of geographic priorities, management options and research needs. Pest. Manag. Sci. 72(6): 1071–1089.

Harvey JA & Malcicka M. 2016. Nutritional integration between insect hosts and koinobiont parasitoids in an evolutionary framework. Entomol. Exp. Appl. 159(2): 181–188.

Islam KS & Copland MJW. 1997. Host preference and progeny sex ratio in a solitary koinobiont mealybug endoparasitoid, Anagyrus pseudococci (Girault), in response to its host stage. Biocontrol Sci. Technol. 7(3): 449–456.

Karamaouna F & Copland M. 2009. Fitness and life history parameters of Leptomastix epona and Pseudaphycus flavidulus, two parasitoids of the obscure mealybug Pseudococcus viburni. BioControl. 54(1): 65–76.

Karmakar P & Shera PS. 2018a. Does host stage affect the morphometry of Aenasius arizonensis (Girault), a solitary endoparasitoid of Phenacoccus solenopsis Tinsley. J. Entomol. Zool. Stud. 6(6): 537–543.

Karmakar P & Shera PS. 2018b. Seasonal and biological interactions between the parasitoid, Aenasius arizonensis (Girault) and its hosts, Phenacoccus solenopsis Tinsley on cotton. Phytoparasitica. 46(5): 661–670.

Khakasa SWR, Mohamed SA, Lagat ZO, Khamis FM, & Tanga CM. 2016. Host stage preference and performance of the aphid parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Brevicoryne brassicae and Lipaphis pseudobrassicae (Hemiptera: Aphididae). Int. J. Trop. Insect Sci. 6(1): 10–21.

King BH. 1987. Offspring sex ratios in parasitoid wasps. Q. Rev. Biol. 62(4): 367–396.

Kraaijeveld AR & van Alphen JJM. 1986. Host-stage selection and sex allocation by Epidinocarsis lopezi (Hymenoptera; Encyrtidae), a parasitoid of the cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae). Meded. Fac. Landbouwwet. Rijksuniv. Gent. 51: 1067–1078.

Le TTN, Graziosi I, Cira TM, Gates MW, Parker L, & Wyckhuys KAG. 2018. Landscape context does not constrain biological control of Phenacoccus manihoti in intensified cassava systems of southern Vietnam. Biol. Control. 121: 129–139.

Li X, Zhu L, Meng L, & Li B. 2017. Brood size and sex ratio in response to host quality and wasp traits in the gregarious parasitoid Oomyzus sokolowskii (Hymenoptera: Eulophidae). PeerJ. 5: e2919.

Luna MG, Desneux N, & Schneider MI. 2016. Encapsulation and self-superparasitism of Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a parasitoid of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). PLoS ONE. 11(10): e0163196.

Mayhew PJ. 2016. Comparing parasitoid life histories. Entomol. Exp. Appl. 159(2): 147–162.

Monticelli LS, Nguyen LTH, Amiens-Desneux E, Luo C, Lavoir AV, Gatti JL, & Desneux N. 2019. The preference-performance relationship as a means of classifying parasitoids according to their specialization degree. Evol. Appl. 12(8): 1626–1640.

Muniappan R, Shepard BM, Watson GW, Carner GR, Rauf A, Sartiami D, Hidayat P, Afun JVK, Goergen G, & Rahman AKMZ. 2009. New records of invasive insects (Hemiptera: Sternorrhyncha) in Southern Asia and West Africa. J. Agric. Urban Entomol. 26(4): 167–174.

Nechols JR & Kikuchi RS. 1985. Host selection of the spherical mealybug (Homoptera: Pseudococcidae) by Anagyrus indicus (Hymenoptera: Encyrtidae): Influence of host stage on parasitoid oviposition, development, sex ratio, and survival. Environ. Entomol. 14(1): 32–37.

Noyes JS & Hayat M. 1994. Oriental Mealybug Parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). CABI, London.

Pacheco da Silva VC, Garcia M, & Botton M. 2017. Biology of Blepyrus clavicornis (Compere) (Hymenoptera: Encyrtidae), a parasitoid of Pseudococcus viburni (Signoret) (Hemiptera: Pseudococcidae). Rev. Bras. Entomol. 61(3): 257–261.

Parsa S, Kondo T, & Winotai A. 2012. The cassava mealybug (Phenacoccus manihoti) in Asia: first records, potential distribution, and an identification key. PLoS ONE 7(10): e47675.

Odebiyi JA & Bokonon-Ganta AH. 1986. Biology of Epidinocarsis [=Apoanagyrus] lopezi [Hymenoptera : Encyrtidae] an exotic parasite cassava mealybug, Phenacoccus manihoti [Homoptera : Pseudococcidae] in Nigeria. Entomophaga. 31(3): 251–260.

Sagarra LA & Vincent C. 1999. Influence of host stage on oviposition, development, sex ratio, and survival of Anagyrus kamali Moursi (Hymenoptera: Encyrtidae), a parasitoid of the Hibiscus mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae). Biol. Control. 15(1): 51–56.

Sarkar MA, Suasa-ard W, & Uraichuen S. 2015. Host stage preference and suitability of Allotropa suasaardi Sarkar & Polaszek (Hymenoptera: Platygasteridae), a newly identified parasitoid of pink cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae). Songklanakarin J. Sci. Techno. 37(4): 381–387.

Schoeller EN & Redak RA. 2018. Host stage preference of Encarsia noyesi, Idioporus affinis, and Entedononecremnus krauteri: parasitoids of the giant whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae). Environ. Entomol. 47(6): 1493–1500.

Shahzad MQ, Abdin ZU, Abbas SK, Tahir M, & Hussain F. 2016. Parasitic effects of solitary endoparasitoid, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae) on cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). Adv. Entomol. 4(2): 90–96.

Stacconi MVR, Buffington M, Daane KM, Dalton DT, Grassi A, Kaçarc G, Miller B, Miller JC, Baser N, Ioriatti C, Walton VM, Wiman NG, Wang X, & Anfora G. 2015. Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol. Control 84: 28–35.

Thancharoen A, Lankaew S, Moonjuntha P, Wongphanuwat T, Sangtongpraow B, Ngoenklan R, Kittipadakul P, & Wykhuys KAG. 2018. Effective biological control of an invasive mealybug pest enhances root yield in cassava. J. Pest Sci. 91(4): 1199–1211.

Ueno T. 2015. Effects of host size and laboratory rearing on offspring development and sex ratio in the solitary parasitoid Agrothereutes lanceolatus (Hymanoptera: Ichneumonidae). Eur. J. Entomol. 112(2): 281–287.

van Dijken JJ & van Alphen JJM. 1991. Sex allocation in Epidinocarsis lopezi: the influence host-size distribution and its effect on the population sex ratio in cassava fields in Africa. Redia. 74(3, Appendix): 195–201.

Vankosky MA & Hoddle MS. 2019. Two parasitoids of Diaphorina citri (Hemiptera: Liviidae) have shared, stage-specific preference for host nymphs that does not impact pest mortality rates. Fla. Entomol. 102(1): 49–58.

Winotai A, Goergen G, Tamò M, & Neuenschwander P. 2010. Cassava mealybug has reached Asia. Biocontrol news and information. 31(2): 10N–11N.

Wyckhuys KAG, Rauf A, & Ketelaar J. 2014. Parasitoid introduced into Indonesia: part of a region-wide campaign to tackle emerging cassava pests and diseases. Biocontrol news and information. 35(4): 35–37.

Wyckhuys KAG, Wongtiem P, Rauf, A, Thancharoen A, Heimpel GE, Le NTT, Fanani MZ, Gurr GM, Lundgren JG, Burra DD, Palao LK, Hyman G, Graziosi I, Le VX, Cock MJW, Tscharntke T, Wratten SD, Nguyen LV, You M, Lu Y, Ketelaar JW, Goergen G, & Neuenschwander P. 2018a. Continental-scale suppression of an invasive pest by a host-specific parasitoid underlines both environmental and economic benefits of arthropod biological control. PeerJ. 6: e5796.

Wyckhuys KAG, Zhang W, Prager SD, Kramer DB, Delaquis E, Gonzalez CE, & van der Werf W. 2018b. Biological control of an invasive pest eases pressures on global commodity markets. Environ. Res. Lett. 13(9): 094005.

Yonow T, Kriticos DJ, & Ota N. 2017. The potential distribution of cassava mealybug (Phenacoccus manihoti), a threat to food security for the poor. PLoS ONE. 12(3): e0173265.

Zhang J, Huang J, Lu Y, & 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. PeerJ. 4(1): e1586.

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(2): 126–129.

Vinson SB & Iwantsch GF. 1980. Host suitability for insect parasitoids. Ann. Rev. Entomol. 25: 397-419.

Waage JK. 1986. Family planning of parasitoids: adaptive patterns of progeny and sex allocation. In: Waage JK & Greathead D (Eds.). Insect Parasitoids. pp. 63–89. Academic Press, London.

Zain-ul-Abdin, Arif MJ, Gogi MD, Arshad M, Hussain F, Abbas SK, Shaina H, & Manzoor A. 2012. Biological characteristics and host stage preference of mealybug parasitoid Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae). Pak. Entomol. 34(1): 47–50.

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2020-09-11
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