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Mosquito diversity (Diptera: Culicidae) and medical importance, in a bird sanctuary inside the flooded forest of Prek Toal, Cambodia

https://doi.org/10.1016/j.aspen.2021.08.001Get rights and content

Highlights

  • Twenty five species of mosquitoes were collected.

  • Culex vishnui represents 58.8% of all collected mosquitoes.

  • Thirteen medically important species are present.

  • Six species could be considered as bridge vectors.

Abstract

Wild birds have been identified as reservoirs of many pathogens transmissible to humans through bird-biting mosquitoes. Understanding the diversity of vector fauna in bird-conservation areas, is a cornerstone to later develop early detection systems and reduce the risk of emerging disease incidence. Prek Toal is a bird Sanctuary in the Tonle-Sap area in Cambodia hosting the largest migratory bird colony of southeast Asia. The Culicidae fauna was investigated during both dry and rainy seasons. In total, 8,224 mosquitoes from 6 genera and 25 species were collected. The two most represented genera were Anopheles (8 species) and Culex (11 species), while the dominant species was Culex vishnui (58.8%). During the rainy season, 1.6 fold more mosquitoes were caught and the number of species doubled. One of the most notable feature is the absence of any Aedinii mosquito which could be attributed to the low human density around the area, and the large populations of migratory birds. A total of 13 species from 3 genera are reported to be of medical importance. 6 medically-important species were collected in all 3 sites, and are known to bite both wild birds and humans: An. barbirostris, An. campestris, Cx. bitaeniorhynchus, Cx. vishnui, Ma. indiana and Ma. uniformis. One of the most important feature is the over-abundance of Culex vishnui, largely dominant in Prek Toal throughout the seasons and the sites, and being present everywhere in Cambodia. This finding stresses its potentiality to act as bridge vectors in the case of new disease emergence.

Introduction

Wild and migratory birds have been identified as reservoirs for many pathogens transmissible to humans and other wildlife through bird-biting mosquitoes (Work et al., 1955, Gern et al., 1998). The interactions between birds and the mosquitoes feeding upon them have been extensively studied (Brown and O'Brien, 2011). Migratory birds can play an important role in virus circulation. This observation emerged from the concomitance of large migratory birds’ arrivals and outbreaks of virus in new areas, but also from virus isolations from these animals. For instance, outbreaks of the West Nile Virus in temperate regions generally occur during late summer or early fall, coinciding with the arrival of large concentrations of migratory birds (and abundance of mosquitoes) (Work et al., 1955, Taylor et al., 1956, Nir et al., 1967, Brown and O'Brien, 2011). Similarly, in the US, both Eastern and Western equine encephalomyelitis alphaviruses, have been isolated from migrating birds highlighting their role in possible local transmission (Lord & Calisher, 1970). It has therefore been hypothesised that migratory birds can act as introductory host, either by infecting blood-sucking arthropods, by direct transmission, by transporting infected vectors during their migration, or by being infected after their arrival at their final landing point (Brown and O'Brien, 2011). In this realm it is fundamental to study the vector diversity, and latter, the virus prevalence in conserved areas playing a role as resting sites in bird migrations.

Located at the north-west corner of the Tonle Sap Lake, in Cambodia, Prek Toal is a Bird Sanctuary (Ramsar site) since 2001, hosting one of the largest migratory bird population in southeast Asia (Campbell et al., 2006). While several mosquito checklists in South-East Asia have been established (for Thailand see Tsukamoto et al., 1987; Rattanarithikul et al., 2005; for Laos: Motoki et al., 2019, and for Vietnam: Bui & Darsie, 2008), over the past few years, yet only partial informations were available for the Cambodian fauna (Harbach, 2021).

In areas like Prek Toal, hosting a rich avifauna −129 species (MoE, 2010) – comprising both resident and migratory birds- and high mosquito diversity, it provides many opportunities for unique ecological relationships among organisms. Furthermore, there are high risks of introduction of new pathogens in bird populations as well as other vertebrates due to migratory birds coming to this area every year. In rapidly changing socio-economic and biophysical environments, particularly in South-East Asia in the context of change in land use, vector-borne diseases can represent a threat for the most vulnerable human populations. Recent pandemic like Zika, Chikungunya, West Nile or Japanese Encephalitis are perfect examples of such recent problems. Yet the Culicidae fauna in conserved areas such as Prek Toal, is still unknown. This knowledge gap is important to fill, considering that change in land use shifts the risk of mosquito-borne disease emergence by changing the relationship between mosquito and host communities both qualitatively and quantitatively (Lourenço-de-Oliveira et al., 2004, Delatte et al., 2010). A modification of the landscape, like deforestation, may facilitate the dispersion of anthropophilic mosquito species into previously unfavorable habitats (Dos Santos et al., 2018) and opportunistic mosquito species may act as bridge vectors. Listing the Culicidae fauna, and its potential vector species is the first step before screening their virome, to be able to properly assess the risk of infectious disease emergence in Prek Toal conserved area.

Section snippets

Collecting permit

This research was allowed by Cambodian authority, with an authorisation letter from the ministry of Environment, issued on 15th November 2019, (Permit N°1443), and an authorisation letter from the Directorate General of Nature Conservation and Protection, issued on the 14th of February 2019 (Permit N°057).

Study sites

Cambodia is largely covered by the Tonle Sap Lake (TSL), which display a very peculiar hydrological regime due to the bisannual reversal flow of the Tonle Sap river into the Mekong. The TSL

Results

The Culicidae fauna collected during the two expeditions is reported in table 1.

In total 8,224 mosquito were collected. About 7.9% (651 specimens) were only identifiable to the genus level. During the study, 25 species were collected, mostly in Culex and Anopheles genus with respectively 11 and 8 species, followed by Mansonia (3 sp), Mimomyia, Ficalbia and Uranotaenia (1 species each). Out of the 260 known species recorded from Cambodia (Harbach, 2021), the sampled mosquitoes in Prek Toal

Discussion

Prek Toal bird sanctuary is characterised by an abundance of Culex mosquitoes throughout the different seasons, accounting for 11 species and 87.74% of collected mosquitoes. The large dominance of Culex spp. is related to their ornithophilic preference and the large presence of birds in the park (Molaei et al., 2010, Chathuranga et al., 2018). Similar observations were made in Sri Lanka by Chathuranga et al. (2018) using bird-baited traps where 52% of their collected mosquitoes were Culex spp.

Conclusion: Importance for public health

Our findings provide baseline information about the risk of emergence of new diseases from wild bird populations to other vertebrates and humans in Cambodia. Prek Toal is an attractive site for migratory birds that can carry pathogens from their migratory routes to Cambodia and vice versa. Several species of medical importance were found across all sites, namely Anopheles barbirostris, An. campestris, Culex bitaeniorhynchus, Cx. vishnui, Mansonia indiana and Ma. uniformis. One of the most

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We would like to thank the rangers from WCS and from Ministry of Environment at the Prek Toal sanctuary bird national park. We also thank Ministry of Environment authorities for approving this study. A special thanks to all the Entomology staff at Institut Pasteur du Cambodge (Sony Yean, Kimly Heng, Kalyan Chhuoy, Sreynik Nhek, Moeun Chhum, Kimhuor Suor) for their assistance during the field and laboratory work.

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