Copulation Activity, Sperm Production and Conidia Transfer in Aedes aegypti Males Contaminated by Metarhizium anisopliae: A Biological Control Prospect

PLoS Negl Trop Dis. 2015 Oct 16;9(10):e0004144. doi: 10.1371/journal.pntd.0004144. eCollection 2015.

Abstract

Background: Dengue is the most prevalent arboviral disease transmitted by Aedes aegypti worldwide, whose chemical control is difficult, expensive, and of inconsistent efficacy. Releases of Metarhizium anisopliae--exposed Ae. aegypti males to disseminate conidia among female mosquitoes by mating represents a promising biological control approach against this important vector. A better understanding of fungus virulence and impact on reproductive parameters of Ae. aegypti, is need before testing auto-dissemination strategies.

Methodology/principal findings: Mortality, mating competitiveness, sperm production, and the capacity to auto-disseminate the fungus to females up to the 5 th copulation, were compared between Aedes aegypti males exposed to 5.96 x 10(7) conidia per cm2 of M. anisopliae and uninfected males. Half (50%) of fungus-exposed males (FEMs) died within the first 4 days post-exposure (PE). FEMs required 34% more time to successively copulate with 5 females (165 ± 3 minutes) than uninfected males (109 ± 3 minutes). Additionally, fungus infection reduced the sperm production by 87% at 5 days PE. Some beneficial impacts were observed, FEMs were able to successfully compete with uninfected males in cages, inseminating an equivalent number of females (about 25%). Under semi-field conditions, the ability of FEMs to search for and inseminate females was also equivalent to uninfected males (both inseminating about 40% females); but for the remaining females that were not inseminated, evidence of tarsal contact (transfer of fluorescent dust) was significantly greater in FEMs compared to controls. The estimated conidia load of a female exposed on the 5th copulation was 5,200 mL(-1) which was sufficient to cause mortality.

Conclusion/significance: Our study is the first to demonstrate auto-dissemination of M. anisopliae through transfer of fungus from males to female Ae. aegypti during mating under semi-field conditions. Our results suggest that auto-dissemination studies using releases of FEMs inside households could successfully infect wild Ae. aegypti females, providing another viable biological control tool for this important the dengue vector.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aedes / microbiology*
  • Aedes / physiology*
  • Animals
  • Colony Count, Microbial
  • Copulation
  • Female
  • Male
  • Metarhizium / isolation & purification*
  • Mosquito Control / methods*
  • Pest Control, Biological / methods*
  • Spermatogenesis
  • Spores, Fungal / isolation & purification*
  • Survival Analysis

Grants and funding

Authors wish to thank Consejo Nacional de Ciencia y Tecnologia of Mexico, grants CB2011-168394 and S008-2013-200664. http://www.conacyt.mx/index.php/fondos-sectoriales-constituidos2/item/ssa-imss-issste-conacyt. They also thank Secretaria de Investigacion y Posgrado (SIP) of the Instituto Politecnico Nacional (IPN), grant 200664. http://www.sappi.ipn.mx/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.