Skip to main content
SpringerLink
Log in

The best time to have sex: mating behaviour and effect of daylight time on male sexual competitiveness in the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Aedes albopictus is the most invasive mosquito worldwide and works as a vector for many important pathogens. Control tools rely to chemical treatments against larvae, indoor residual spraying and insecticide-treated bed nets. Recently, huge efforts have been carried out to propose new eco-friendly alternatives, such as evaluation of plant-borne compounds and sterile insect technique (SIT) programs. Success of SIT is dependent to the ability of sterile males to compete for mates with wild ones. Little is still known about mating behaviour of Aedes males. Most of the studies focus on comparisons of insemination ability in sterilised and wild males, while behavioural analyses of mating behaviour are lacking. Here, I quantified the courtship and mating behaviour of A. albopictus and evaluated how daylight hours affect male mating behaviour and success. A. albopictus males chased females facing them frontally, from behind, or from a lateral side. If the female allowed genital contact, copulation followed. Otherwise, females performed rejection kicks and/or flew away. Thirty-seven percent of males obtained a successful copulation (i.e. sperm transfer occurs), lasting 63 ± 4 s. Unsuccessful copulation (20 % of males) had shorter duration (18 ± 1 s). Successful copulations followed longer male courtships (39 ± 3 s), over courtships preceding unsuccessful copulation (20 ± 2 s) or male’s rejection (22 ± 2 s). After copulation, the male rested 7 ± 0.4 s close to the female, then move off. In a semi-natural environment, male mating success was lower in early afternoon, over morning and late afternoon. However, little differences in courtship duration over daylight periods were found. This study adds knowledge to the reproductive behaviour of A. albopictus, which can be used to perform comparisons among courtship and mating ethograms from different mosquito species and strains, allowing monitoring and optimisation of mass rearing quality over time in SIT programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amer A, Mehlhorn H (2006a) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472

    Article  PubMed  Google Scholar 

  • Amer A, Mehlhorn H (2006b) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490

    Article  PubMed  Google Scholar 

  • Assogba BS, Djogbénou L, Saizonou J, Diabaté A, Dabire RK, Gilles J, Makoutode M, Baldet T (2014) Characterization of swarming and mating behaviour between Anopheles coluzzii and Anopheles melas in a sympatry area of Benin. Acta Trop 132S:S53–S63

    Article  Google Scholar 

  • Balestrino F, Medici A, Candini G, Carrieri M, Maccagnani B, Calvitti M, Maini S, Bellini R (2010) γ ray dosimetry and mating capacity studies in the laboratory on Aedes albopictus males. J Med Entomol 47:581–591

    PubMed  CAS  Google Scholar 

  • Bargielowski I, Alphey L, Koella JC (2011) Cost of mating and insemination capacity of a genetically modified mosquito Aedes aegypti OX513A compared to its wild type counterpart. PLoS ONE 6:e26086

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bellini R, Balestrino F, Medici A, Gentile G, Veronesi R, Carrieri M (2013) Mating competitiveness of Aedes albopictus radio-sterilized males in large enclosures exposed to natural conditions. J Med Entomol 50:94–102

    Article  PubMed  CAS  Google Scholar 

  • Bellini R, Puggioli A, Balestrino F, Brunelli P, Medici A, Urbanelli S, Carrieri M (2014) Sugar administration to newly emerged Aedes albopictus males increases their survival probability and mating performance. Acta Trop 132S:S116–S123

    Article  CAS  Google Scholar 

  • Benedict MQ, Levine RS, Hawley WA, Lounibos LP (2007) Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vect Bor Zoon Dis 7:76–85

    Article  Google Scholar 

  • Benelli G (2014) Aggressive behavior and territoriality in the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae): role of residence and time of day. J Insect Behav 27:145–161

    Article  Google Scholar 

  • Benelli G, Conti B, Garreffa R, Nicoletti M (2014a) Shedding light on bioactivity of botanical by-products: neem cake compounds deter oviposition of the arbovirus vector Aedes albopictus (Diptera: Culicidae) in the field. Parasitol Res 113:933–940

    Article  PubMed  Google Scholar 

  • Benelli G, Bedini S, Cosci F, Toniolo C, Conti B, Nicoletti M (2014b) Larvicidal and ovideterrent properties of neem oil and fractions against the filariasis vector Aedes albopictus (Diptera: Culicidae): a bioactivity survey across production sites. Parasitol Res. doi:10.1007/s00436-014-4183-3

    Google Scholar 

  • Benelli G, Daane KM, Canale A, Niu CY, Messing RH, Vargas RI (2014c) Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for integrated pest management. J Pest Sci 87:385–405

    Article  Google Scholar 

  • Benelli G, Stefanini C, Giunti G, Geri S, Messing RH, Canale A (2014d) Associative learning for danger avoidance nullifies innate positive chemotaxis to host olfactory stimuli in a parasitic wasp. Naturwissenschaften 101:753–757

    Article  PubMed  CAS  Google Scholar 

  • Bonizzoni M, Gasperi G, Chen X, James A (2013) The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol 29:460–468

    Article  PubMed Central  PubMed  Google Scholar 

  • Bowatte G, Perera P, Senevirathne G, Meegaskumbura S, Meegaskumbura M (2013) Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biol Control 67:469–474

    Article  Google Scholar 

  • Boyer S, Gilles J, Meracienne D, Lemperiere G, Fontenille D (2011) Sexual performance of male mosquito Aedes albopictus. Med Vet Entomol 25:454–459

    Article  PubMed  CAS  Google Scholar 

  • Butail S, Manoukis NC, Diallo M, Ribeiro J, Lehmann T, Paley D (2012) Reconstructing the flight kinematics of swarming and mating behaviour in wild mosquitoes. J R Soc Interface 7:2624–2638

    Article  Google Scholar 

  • Cabrera M, Jaffe K (2007) An aggregation pheromone modulates lekking behavior in the vector mosquito Aedes aegypti (Diptera: Culicidae). J Am Mosq Contr Assoc 23:1–10

    Article  Google Scholar 

  • Caminade C, Medlock JM, Ducheyne E, McIntryre KM, Leach S, Baylis M, Morse A (2012) Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. J R Soc Interface 9:2708–2717

    Article  PubMed Central  PubMed  Google Scholar 

  • Cator LJ, Harrington LC (2010) The harmonic convergence of fathers predicts the mating success of sons in Aedes aegypti. Anim Behav 82:627–633

    Article  Google Scholar 

  • Cator LJ, Harrington LC (2011) Harmonic convergence of fathers and the mating success of sons in the yellow fever mosquito. Anim Behav 82:627–633

  • Chadee DD, Gilles JRL (2014) The diel copulation periodicity of the mosquito, Aedes aegypti (L.) (Diptera: Culicidae) at indoor and outdoor sites in Trinidad, West Indies. Acta Trop 132S:S91–S95

    Article  Google Scholar 

  • Charlwood JD, Jones MDR (1979) Mating behaviour in the mosquito Anopheles gambiae s.l. save. Physiol Entomol 4:111–120

    Article  Google Scholar 

  • Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C, do Rosario VE (2002) The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tomé Island. J Vector Ecol 27:178–183

    PubMed  CAS  Google Scholar 

  • Charlwood JD, Thompson R, Madsen H (2003) Observations on the swarming and mating behaviour of Anopheles funestus from Sourthern Mozambique. Malaria J 2:2

    Article  CAS  Google Scholar 

  • Conti B, Flamini G, Cioni PL, Ceccarini L, Macchia M, Benelli G (2014) Mosquitocidal essential oils: are they safe against non-target aquatic organisms? Parasitol Res 113:251–259

    Article  PubMed  Google Scholar 

  • Dabiré KR, Sawadogo PS, Hien DF, Maiga H, Millogo A, Baldet T, Simard F, Gouagna L-C, Diabate A, Gibson G, Lees RS, Gilles JRL (2014) Occurrence of natural Anopheles arabiensis swarms in an urban area of Bobo-Dioulasso city, Burkina Faso, West Africa. Acta Trop 132S:S35–S41

    Article  Google Scholar 

  • Downes JA (1966) Observations on the mating behaviour of the crab hole mosquito Deinocerites cancer (Diptera: Culicidae). Can Entomol 98:1169–1177

    Article  Google Scholar 

  • Gubler D, Bhattacharya N (1972) Swarming and mating of Aedes (S.) albopictus in nature. Mosq News 32:219–223

    Google Scholar 

  • Hamady D, Ruslan NB, Ahmad AH, Rawi CSM, Hamad H, Satho T et al (2013) Colonized Aedes albopictus and its sexual performances in the wild: implications for SIT technology and containment. Parasit Vectors 6:206

    Article  PubMed Central  PubMed  Google Scholar 

  • Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391

    Article  PubMed  CAS  Google Scholar 

  • Jensen M, Mehlhorn H (2009) Seventy-five years of Resochin® in the fight against malaria. Parasitol Res 105:609–627

    Article  PubMed  Google Scholar 

  • Jones MDR (1981) The programming of circadian flight-activity in relation to mating and the gonotrophic cycle in the mosquito Aedes aegypti. Physiol Entomol 6:307–313

    Article  Google Scholar 

  • Lees RS, Knols B, Bellini R, Benedict MQ, Bheecarry A, Bossin HC et al (2014) Review: Improving our knowledge of male mosquito biology in relation to genetic control programmes. Acta Trop 132S:S2–S11

    Article  Google Scholar 

  • Madakacherry O, Lees RS, Gilles JRL (2014) Aedes albopictus (Skuse) males in laboratory and semi-field cages: release ratios and mating competitiveness. Acta Trop 132S:124–129

    Article  Google Scholar 

  • Maïga H, Niang A, Sawadogo SP, Dabiré RK, Lees RS, Gilles JRL, Tripet F, Diabaté A (2014) Role of nutritional reserves and body size in Anopheles gambiae males mating success. Acta Trop 132S:S102–S107

    Article  Google Scholar 

  • Moretti R, Calvitti M (2013) Male mating performance and cytoplasmic incompatibility in a wPip Wolbachia trans-infected line of Aedes albopictus (Stegomyia albopicta). Med Vet Entomol 27:377–386

    Article  PubMed  CAS  Google Scholar 

  • O’Connor L, Plichart C, Sang AC, Brelsfoard CL, Bossin HC, Dobson SL (2012) Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment. PLoS Negl Trop Dis 6:e4797

    Google Scholar 

  • Oliva CF, Jacquet M, Gilles J, Lemperiere G, Maquart PO, Quilici S, Schooneman F, Vreysen MJB, Boyer S (2012) The sterile insect technique for controlling populations of Aedes albopictus (Diptera: Culicidae) on Reunion Island: mating vigour of sterilized males. PLoS ONE 7:e49414

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Oliva CF, Damiens D, Vreysen MJB, Lemperière GJ (2013) Reproductive strategies of Aedes albopictus (Diptera: Culicidae) and implications for the sterile insect technique. PLoS ONE 8:e78884

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Oliva CF, Damiens D, Benedict MQ (2014) Male reproductive biology of Aedes mosquitoes. Acta Trop 132S:S512–S519

    Google Scholar 

  • Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D (2009) Aedes albopictus, an arbovirus vector: from the darkness to light. Microb Infect 11:1177–1185

    Article  CAS  Google Scholar 

  • Pennetier C, Warren B, Dabiré R, Russell IJ, Gibson G (2010) “Singing on the wing” as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr Biol 20:131–136

    Article  PubMed  CAS  Google Scholar 

  • Philips KT, Hancock RG, Foster WA (1996) Epigamic display and unique mating position in Wyeomyia arthrostigma (Diptera: Culicidae). J Insect Behav 9:739–753

    Article  Google Scholar 

  • Pitts RJ, Mozūraitis R, Gauvin-Bialecki A, Lempérière G (2014) The roles of kairomones, synomones and pheromones in the chemically-mediated behaviour of male mosquitoes. Acta Trop 132S:S26–S34

    Article  CAS  Google Scholar 

  • Provost MW, Haeger JS (1967) Mating and pupal attendance in Deinocerites cancer and comparisons with Opifex fuscus (Diptera: Culicidae). Ann Entomol Soc Am 60:565–574

    Article  Google Scholar 

  • Sawadogo P, Diabaté A, Sanon A, Toé H, Baldet T, Gibson G, Gilles J, Simard F, Sinkins S, Dabiré K (2013) Effects of age and size on Anopheles gambiae s.s. male mosquito mating success. J Med Entomol 50:285–293

    Article  PubMed  Google Scholar 

  • Semmler M, Abdel-Ghaffar F, Schmidt J, Mehlhorn H (2014) Evaluation of biological and chemical insect repellents and their potential adverse effects. Parasitol Res 113:185–188

    Article  PubMed  Google Scholar 

  • South SH, Arnqvist G (2008) Evidence of monandry in a mosquito (Sabethes cyaneus) with elaborate ornaments in both sexes. J Insect Behav 21:451–459

    Article  Google Scholar 

  • South SH, Steiner D, Arnqvist G (2009) Male mating costs in a polygynous mosquito with ornaments expressed in both sexes. Proc R Soc B 276:3671–3678

  • South SH, Arnqvist G (2011) Male, but not female, preference for an ornament expressed in both sexes of the polygynous mosquito Sabethes cyaneus. Anim Behav 81:645–651

    Article  Google Scholar 

  • Wiwatanaratanabutr I, Allan S, Linthicum K, Kittayapong P (2010) Strain-specific differences in mating, oviposition, and host-seeking behaviour between Wolbachia-infected and uninfected Aedes albopictus. J Am Mosq Contr Assoc 26:265–273

    Article  CAS  Google Scholar 

  • Yuval B, Bouskilla A (1993) Temporal dynamics of mating and predation in mosquito swarms. Oecologia 95:65–69

    Article  Google Scholar 

  • Zsemlye JL, Hancock RG, Foster WA (2005) Analysis of a complex vertical copulatory-courtship display in the yellow fever vector Sabethes chloropterus. Med Vet Entomol 19:276–285

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I am grateful to Professor Heinz Mehlhorn and the anonymous reviewers for their comments on an earlier version of the manuscript. I would like to thank Barbara Conti for providing A. albopictus specimens and Donato Romano for assistance in behavioural observations. I am supported by a MIS. 124 MODOLIVI Grant. Funds were also provided by the Italian Ministry of Education, University and Research (MIUR). Funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Disclosure

The author did not have potential conflict of interests relevant to the subject of this research.

Author information

Authors and Affiliations

  1. Insect Behaviour Group, Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124, Pisa, Italy

    Giovanni Benelli

Authors
  1. Giovanni Benelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giovanni Benelli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Benelli, G. The best time to have sex: mating behaviour and effect of daylight time on male sexual competitiveness in the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae). Parasitol Res 114, 887–894 (2015). https://doi.org/10.1007/s00436-014-4252-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4252-7

Keywords

Search

Navigation