The Biting Midge Culicoides sonorensis (Diptera: Ceratopogonidae) Is Capable of Developing Late Stage Infections of Leishmania enriettii

Abstract

Background

Despite their importance in animal and human health, the epidemiology of species of the Leishmania enriettii complex remains poorly understood, including the identity of their biological vectors. Biting midges of the genus Forcipomyia (Lasiohelea) have been implicated in the transmission of a member of the L. enriettii complex in Australia, but the far larger and more widespread genus Culicoides has not been investigated for the potential to include vectors to date.

Methodology/Principal Findings

Females from colonies of the midges Culicoides nubeculosus Meigen and C. sonorensis Wirth & Jones and the sand fly Lutzomyia longipalpis Lutz & Nevia (Diptera: Psychodidae) were experimentally infected with two different species of Leishmania, originating from Australia ( Leishmania sp. AM-2004) and Brazil ( Leishmania enriettii). In addition, the infectivity of L. enriettii infections generated in guinea pigs and golden hamsters for Lu. longipalpis and C. sonorensis was tested by xenodiagnosis. Development of L. enriettii in Lu. longipalpis was relatively poor compared to other Leishmania species in this permissive vector. Culicoides nubeculosus was not susceptible to infection by parasites from the L. enriettii complex. In contrast, C. sonorensis developed late stage infections with colonization of the thoracic midgut and the stomodeal valve. In hamsters, experimental infection with L. enriettii led only to mild symptoms, while in guinea pigs L. enriettii grew aggressively, producing large, ulcerated, tumour-like lesions. A high proportion of C. sonorensis (up to 80%) feeding on the ears and nose of these guinea pigs became infected.

Conclusions/Significance

We demonstrate that L. enriettii can develop late stage infections in the biting midge Culicoides sonorensis. This midge was found to be susceptible to L. enriettii to a similar degree as Lutzomyia longipalpis, the vector of Leishmania infantum in South America. Our results support the hypothesis that some biting midges could be natural vectors of the L. enriettii complex because of their vector competence, although not Culicoides sonorensis itself, which is not sympatric, and midges should be assessed in the field while searching for vectors of related Leishmania species including L. martiniquensis and " L. siamensis".

Author Summary

This study investigates the laboratory infection of two species of Culicoides biting midges (Diptera: Ceratopogonidae) and one species of sand fly (Diptera: Psychodidae) with two species of Leishmania. These members of the L. enriettii complex were demonstrated to colonize the stomodeal valve of Culicoides sonorensis following membrane feeding on blood-parasite mixtures or direct feeding on guinea pigs that demonstrated clinical signs of infection. In contrast, three other species of Leishmania that are known to be transmitted by sand flies failed to successfully develop in C. sonorensis. A sand fly species which is highly permissive to Leishmania infection, Lu. longipalpis, a widespread vector of L. infantum in Latin America, was found to support only moderate infections of L. enriettii from Brazil and Leishmania sp. AM-2004 from Australia. In addition to establishing a suitable laboratory model for infection of Culicoides with L. enriettii, successful infection of C. sonorensis highlights that vectors other than sand flies should be considered as part of epidemiological studies on parasites belonging to the L. enriettii complex.