Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-19T02:31:18.163Z Has data issue: false hasContentIssue false
  • English
  • Français

Biparental mealybugs may be more promiscuous than we thought

Published online by Cambridge University Press:  31 October 2018

E.B. Silva Open the ORCID record for E.B. Silva [Opens in a new window] ,
C. Mourato Open the ORCID record for C. Mourato [Opens in a new window] ,
M. Branco Open the ORCID record for M. Branco [Opens in a new window] ,
Z. Mendel  and
J.C. Franco Open the ORCID record for J.C. Franco [Opens in a new window]
E.B. Silva*
Affiliation:
Centro de Estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal
C. Mourato
Affiliation:
Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal
M. Branco
Affiliation:
Centro de Estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal
Z. Mendel
Affiliation:
Department of Entomology, Volcani Center, ARO, Bet Dagan 50250, Israel
J.C. Franco
Affiliation:
Centro de Estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal
*
*Author for correspondence Phone: +21.3653220 Fax: +21.3653430 E-mail: elsasilva@isa.ulisboa.pt
Get access Rights & Permissions [Opens in a new window]

Abstract

Knowledge on the reproductive biology of target insect pest is essential for the effective implementation of pheromone-based pest management tactics. In mealybugs, the second largest family of scale insects, the existence of female multiple mating was recently suggested. In this study, we aimed at testing how general is this behavior in mealybugs, by investigating polygyny and polyandry in two cosmopolitan pest mealybugs, Planococcus citri and Pseudococcus calceolariae. Males of these species were able to mate an average of 11.9 and 13.3 females, respectively, during their lifespan. The number of fertilized females per male decreased with male age/mating history for both mealybugs. We found no differences in female fecundity and fertility, when fertilized by males with different mating history. When we used male age as a proxy of mating history, we observed a significant negative effect on female fecundity. The females of both species remained receptive after first copula and eventually mated multiple times. The percentage of remated females of P. citri decreased linearly with time since first copula, with some maintaining receptivity up to 24 h. Males showed no preference between virgin and mated females, in static-air olfactometer tests. We found no benefit of female multiple mating in relation to fecundity. In biparental mealybugs, the mating system of males is possibly scramble competition polygyny; and that of females is possibly polyandry, with female receptivity restricted to a relatively short period. We discuss the practical implications of the results for pest management.

Keywords

polyandrypolygynymating systemPlanococcus citriPseudococcus calceolariae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 5 , October 2019 , pp. 574 - 582
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnqvist, G. & Andres, J.A. (2006) The effects of experimentally induced polyandry on female reproduction in a monandrous mating system. Ethology 112, 748–756.Google Scholar
Arnqvist, G. & Nilsson, T. (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145–164.Google Scholar
Bierl-Leonhardt, B.A., Moreno, D.S., Schwarz, M., Fargerlund, J. & Plimmer, J.R. (1981) Isolation, identification and synthesis of the sex-pheromone of the citrus mealybug, Planococcus citri (Risso). Tetrahedron Letters 22, 389–392.Google Scholar
Boake, C.R.B., Shelly, T.E. & Kaneshiro, K.Y. (1996) Sexual selection in relation to pest-management strategies. Annual Review of Entomology 41, 211–229. PubMed: 15012328.Google Scholar
Cocco, A., Lentini, A. & Serra, G. (2014) Mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in vineyards using reservoir pheromone dispensers. Journal of Insect Science 14, 1–8.Google Scholar
Correa, M., Zaviezo, T., Le Maguet, J., Herrbach, E. & Malausa, T. (2014) Characterization of microsatellite DNA libraries from three mealybug species and development of microsatellite markers for Pseudococcus viburni (Hemiptera: Pseudococcidae). Bulletin of Entomological Research 104, 213–220.Google Scholar
Cox, J.M. & Pearce, M.J. (1983) Wax produced by dermal pores in three species of mealybug (Homoptera, Pseudococcidae). International Journal of Insect Morphology and Embryology 12, 235–248.Google Scholar
El-Minshawy, A.M., Karan, H.H. & El-Sawaf, S.K. (1974) Biological studies on the long tailed mealybug Pseudococcus longispinus (Targ. and Tozzeti). Bulletin of Entomological Society of Egypt 58, 385–391.Google Scholar
El-Sayed, A.M. (2017) The Pherobase: Database of Insect Pheromones and Semiochemicals. Available online at http://www.pherobase.com (accessed 5 March 2018).Google Scholar
El-Sayed, A.M., Unelius, C.R., Twidle, A., Mitchell, V., Manning, L.A., Cole, L., Suckling, D.M., Flores, M.F., Zaviezo, T. & Bergmann, J. (2010) Chrysanthemyl 2-acetoxy-3-methylbutanoate: the sex pheromone of the citrophilous mealybug Pseudococcus calceolariae. Tetrahedron Letters 51, 1075–1078.Google Scholar
Foldi, I. (1983) Structure and functions of the integumentary glands of mealybugs Pseudococcidae and of their secretions. Annals of Society Entomological of France 19, 155–166.Google Scholar
Franco, J.C. & Marotta, S. (1999) A survey of the mealybugs in citrus groves in Portugal. Entomologica 33, 191–196.Google Scholar
Franco, J.C., Gross, S., Silva, E.B., Suma, P., Russo, A. & Mendel, Z. (2004) Is mass-trapping a feasible management tactic of the citrus mealybug in citrus orchards? Anais do Instituto Superior de Agronomia 49, 353–367.Google Scholar
Franco, J.C., Zada, A. & Mendel, Z. (2009) Novel approaches for the management of mealybug pests. pp. 233–278 in Ishaaya, I. & Horowitz, A.R. (Eds) Biorational Control of Arthropod Pests: Application and Resistance Management, Dordrecht, The Netherlands, Springer.Google Scholar
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 systematics. Database. doi: https://doi:10.1093/database/bav118. Available online at http://scalenet.info (accessed 5 March 2018).Google Scholar
Gowaty, P.A. (2012) The evolution of multiple mating. Costs and benefits of polyandry to females and of polygyny to males. Fly 6, 3–11.Google Scholar
Gullan, P.J. & Kosztarab, M. (1997) Adaptations in scale insects. Annual Review of Entomology 42, 23–50.Google Scholar
Hosken, D. & Stockley, P. (2003) Benefits of polyandry: a life history perspective. Evolutionary Biology 33, 173–194.Google Scholar
James, H.C. (1937) Sex ratios and the status of the male in pseudococcinae (Hem, Coccidae). Bulletin of Entomological Research 28, 429–461.Google Scholar
Jennions, M.D. & Petrie, M. (2000) Why do females mate multiply? A review of the genetic benefits. Biological Reviews 75, 21–64.Google Scholar
King, B.H. & Fischer, C.R. (2010) Male mating history: effects on female sexual responsiveness and reproductive success in the parasitoid wasp Spalangia endius. Behavioral Ecology and Sociobiology 64, 607–615.Google Scholar
Lanier, G.N. (1990) Principles of attraction-annihilation: mass trapping and other means. pp. 25–45 in Ridgway, R.L., Silverstein, R.M. & Inscoe, M.N. (Eds) Behavior-modifying Chemicals for Insect Management. Applications of Pheromones and Other Attractants, New York, Marcel Dekker Inc.Google Scholar
Lauwers, K. & van Dyck, H. (2006) The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood, Pararge aegeria. Behavioral Ecology and Sociobiology 60, 69–76.Google Scholar
Lentini, A., Mura, A., Muscas, E., Nuvoli, M. & Cocco, A. (2017) Effects of delayed mating on the reproductive biology of the vine mealybug, Planococcus ficus (Hemiptera: Pseudococcidae). Bulletin of Entomological Research 6, 1–8.Google Scholar
Levi-Zada, A., Fefer, D., David, M., Eliyahu, M., Franco, J.C., Protasov, A., Dunkelblum, E. & Mendel, Z. (2014) Diel periodicity of pheromone release by females of Planococcus citri and Planococcus ficus and the temporal flight activity of their conspecific males. Naturwissenschaften 101, 671–678.Google Scholar
Marcotte, M., Delisle, J. & McNeil, J.N. (2007) Effects of different male remating intervals on the reproductive success of Choristoneura rosaceana males and females. Journal of Insect Physiology 53, 139–145.Google Scholar
Martens, A. & Rehfelt, G. (1989) Female aggregation in Platycypha caligata (Odonata: Chlorocipidae): a tactic to evade male interference during oviposition. Animal Behaviour 38, 369–374.Google Scholar
Martins, R.F., Zina, V., Silva, E.B., Rebelo, M.T., Figueiredo, E., Mendel, Z., Paulo, O.S., Franco, J.C. & Seabra, S.G. (2012) Isolation and characterization of fifteen polymorphic microsatellite loci for the citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae), and cross-amplification in two other mealybug species. Journal of Genetics 91, e75–e78. Available online at http://www.ias.ac.in/article/fulltext/jgen/091/online/e0075-e0078.Google Scholar
Mendel, Z., Protasov, A., Jasrotia, P., Silva, E.B., Levi-Zada, A. & Franco, J.C. (2012) Sexual maturation and aging of adult male mealybugs (Hemiptera; Pseudococcidae). Bulletin of Entomological Research 102, 385–394.Google Scholar
Millar, J.G., Daane, K.M., McElfresh, J.S., Moreira, J. & Bentley, W.J. (2005) Chemistry and applications of mealybug sex pheromones. pp. 11–27 in Petroski, R.J., Tellez, M.R. & Behle, R.W. (Eds) Semiochemicals in Pest and Weed Control, Washington, DC, American Chemical Society.Google Scholar
Miyatake, T., Chapman, T. & Partridge, L. (1999) Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. Journal of Insect Physiology 45, 1021–1028.Google Scholar
Nelson-Rees, W.A. (1959) Triple coitus in the Mealy Bug, Planococcus citri (Risso). Nature 183, 479.Google Scholar
Nestel, D., Cohen, H., Saphir, N., Klein, M. & Mendel, Z. (1995) Spatial distribution of scale insects: comparative study using Taylor's power law. Environmental Entomology 24, 506–512.Google Scholar
Panis, A. (1969) Observations faunistiques et biologiques sur quelques Pseudococcidae (Homoptera, Coccoidea) vivant dans le midi de la France. Annales de Zooogie et Ecologie Animale 1, 211–244.Google Scholar
Rowe, L. (1992) Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Animal Behaviour 44, 189–202.Google Scholar
Seabra, S.G., Brás, P.G., Zina, V., Silva, E.B., Rebelo, M.T., Figueiredo, E., Mendel, Z., Paulo, O.S. & Franco, J.C. (2013) Molecular evidence of polyandry in the citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). PLoS ONE 8(7), e68241.Google Scholar
Sharon, R., Zahavi, T., Sokolsky, T., Sofer-Arad, C., Tomer, M., Kedoshim, R. & Harari, A.R. (2016) Mating disruption method against the vine mealybug, Planococcus ficus: effect of sequential treatment on infested vines. Entomologia Experimentalis et Applicata 161, 65–69.Google Scholar
Silva, E.B., Mouco, J., Antunes, R., Mendel, Z. & Franco, J.C. (2009) Mate location and sexual maturity of adult male mealybugs: narrow window of opportunity in a short lifetime. IOBC WRPS Bulletin 4, 3–9.Google Scholar
Silva, E.B., Branco, M., Mendel, Z. & Franco, J.C. (2013) Mating behavior and performance in the two cosmopolitan mealybug species Planococcus citri and Pseudococcus calceolariae (Hemiptera: Pseudococcidae). Journal of Insect Behavior 3, 304–320.Google Scholar
Suckling, D.M. (2000) Issues affecting the use of pheromones and other semiochemicals in orchards. Crop Protection 19, 677–683.Google Scholar
Thornhill, R. & Alcock, J. (2001) The Evolution of Insect Mating Systems. Lincoln, EUA, iUniverse.com Inc, 547pp.Google Scholar
Torres-Vila, L.M. & Jennions, M.D. (2005) Male mating history and female fecundity in the Lepidoptera: do male virgins make better partners? Behavioral Ecology and Sociobiology 57, 318–326.Google Scholar
Vet, L.E.M. (1983) Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym.: Eucoilidae), a parasitoid of fungivorous Drosophila: the influence of conditioning. Netherlands Journal of Zoology 33, 225–248.Google Scholar
Waterworth, R.A. & Millar, J.G. (2012) Reproductive biology of Pseudococcus maritimus (Hemiptera: Pseudococcidae). Journal of Economic Entomology 105, 949–956.Google Scholar
Waterworth, R.A., Wright, I.M. & Millar, J.G. (2011) Reproductive biology of three cosmopolitan mealybug (Hemiptera: Pseudococcidae) species, Pseudococcus longispinus, Pseudococcus viburni, and Planococcus ficus. Annals of Entomological Society of America 104, 249–260.Google Scholar
Wedell, N. (1997) Ejaculate size in bushcrickets: the importance of being large. Journal of Evolutionary Biology 10, 315–325.Google Scholar
Wedell, N. (2005) Female receptivity in butterflies and moths. Journal of Experimental Biology 208, 3433–3440.Google Scholar
Zada, A., Dunkelblum, E., Assael, F., Franco, J.C., Silva, E.B., Protasov, A. & Mendel, Z. (2008) Attraction of Planococcus ficus males to racemic and chiral pheromone baits: flight activity and bait longevity. Journal of Applied Entomology 132, 480–489.Google Scholar