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A video clip of the biting midge Culicoides anophelis ingesting blood from an engorged Anopheles mosquito in Hainan, China

Yajun Ma1*, Jiannong Xu2*, Zhenzhou Yang3*, Xiaohua Wang4, Zhongling Lin4, Wei Zhao5, Yan Wang1, Xiangyu Li1 and Hua Shi3

Author Affiliations

1 Department of Tropical Infectious Diseases, Second Military Medical University, 800 Xiangyin Road, 200433 Shanghai, China

2 Department of Biology, New Mexico State University, PO Box 30001 MSC 3AF, Las Cruces, NM 88003, USA

3 Center for Disease Control and Prevention of P.L.A, 20 Dongdajie Road Fengtai District, 100071 Beijing China

4 Center for Disease Control and Prevention of Haikou City, Haikou, Hainan, China

5 Center for Disease Control and Prevention of Hainan Province, Haikou, Hainan, China

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Parasites & Vectors 2013, 6:326  doi:10.1186/1756-3305-6-326

The electronic version of this article is the complete one and can be found online at: http://www.parasitesandvectors.com/content/6/1/326


Received:23 October 2013
Accepted:11 November 2013
Published:13 November 2013

© 2013 Ma et al.; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Abstract

Background

Biting midges are hematophagus ectoparasites of insects, humans and other animals. Culicoides (Trithicoides) anophelis Edwards1922 is a predator of engorged mosquitoes.

Findings

In a field trip of wild mosquito collections, C. anophelis was found on two Anopheles mosquitoes. One mosquito with a midge clinging onto its abdomen was caught on video demonstrating the act of the midge taking blood from the engorged mosquito Anopheles vagus. The midge C. anophelis has a broad host range. Documented in the literature, the midge has been found in various mosquito species in the genera Anopheles, Culex, Aedes and Armigeres.

Conclusions

A video clip was presented demonstrating a midge taking blood from an engorged mosquito. The host promiscuity of C. anophelis raises a concern about its potential as a mechanic or biological vector to spread viruses among mosquito populations.

Keywords:
Culicoides anophelis; Anopheles mosquito; Biting midge; Video

Findings

The biting midge Culicoides (Trithecoides) anophelis Edwards is a predator of engorged mosquitoes, which was first described by Edwards in 1922 [1]. Later in 1947, Liard reported a C. anophelis sucking engorged blood from the abdomen of a flying mosquito Armigeres lacuum[2]. In the 1950s, C. anophelis was found on the mosquitoes in the genera Aedes, Anopheles, Armigeres and Culex mosquitoes in Hainan, China [3]. There are several reports of the midge in India [4,5]. Here we report two anopheline mosquitoes that were attacked by C. anophelis, and one scene was caught on video demonstrating the act of a midge taking blood from an engorged mosquito.

The observation was made in the course of a mosquito collection on the evening of August 10, 2013 in Yanfeng, Haikou, Hainan Province, China. Mosquitoes were attracted and trapped in a net trap inside which a cow was placed. The trapped mosquitoes were caught by an electronic aspirator and released into a cage and brought back to the laboratory for further processing. When sorting out mosquitoes, one mosquito was found to have a midge clinging to its abdomen (Figure 1). The mosquito was identified as Anopheles sinensis and the midge was identified as C. anophelis. The next day, another mosquito collection was carried out using the same baited trap. Among the mosquitoes collected, another mosquito was found carrying a midge. The mosquito and midge were chloroformed lightly, the mosquito was immobilised and the midge was active and hanging onto the mosquito abdomen. The mosquito and midge were placed under a stereo microscope (Nickon SMZ745T). A video was recorded with a camera (Additional file 1). On the video footage, the midge firmly attached itself to the mosquito via the mouthparts that had penetrated the lateral part of the fourth segment of the engorged abdomen. The midge abdomen distended with blood in it. Periodically the legs were moving agitatedly. About 3 minutes later, the midge was trying to remove its mouthparts from the mosquito. It appeared difficult to unplug the proboscis, the midge rotated 180° with the mouthparts inside the abdomen and finally detached from the mosquito. The steady attachment may be attributed to the structure of the mouthparts [6,7], which ensures that midges can hang onto flying mosquitoes while ingesting blood. Documented by Edwards (1922) and Chhila and Chaudhry (2010), the midge could remain attached to its host mosquito for 48–56 hr [1,4]. The mosquito was identified as An. vagus, and the midge was identified as C. anophelis by morphology [1].

thumbnailFigure 1. A midge of Culicoides anophelis attached to the abdomen of the mosquito Anopheles sinensis.

Additional file 1. A midge Culicoides anophelis is ingesting blood from an engorged mosquito Anopheles vague.

Format: RAR Size: 16.3MB Download fileOpen Data

At least 19 mosquito species in the genera Anopheles, Culex, Aedes and Armigeres have been documented as hosts of C. anophelis (Table 1). These data indicate that C. anophelis has a broad host range. Furthermore, the infestation is commonly seen in the mosquito specimens in field collections [1-3]. In a recent report the midges were found on 8 of 11 (72.7%) An. stephensi collected in cattle sheds in India [4]. In another report from India, the prevalence of C. anophelis was 6.7% (87/1297) in five midge collections from April to August in 2004 [5]. Interestingly, in the same report, some of C. anophelis were caught directly on cattle and buffaloes, which indicates that C. anophelis can feed on animals other than mosquitoes [5]. Certain mosquitoes and Culicoides midges are vectors for arboviruses that cause human and/or animal diseases, such as mosquito-borne Dengue virus, West Nile virus, Japanese encephalitis virus, and midge-borne bluetongue virus, Oropouche virus and Schmallenberg virus [8-10]. The fact that C. anophelis takes blood from a broad range of mosquitoes raised a concern that the midge may serve as a mechanism for biological vectors to spread viruses among mosquito populations. However, to the best of our knowledge, except the mosquito infestation reports, little is known about the behavior, ecology and genetics of C. anophelis. No data are available regarding the vector potentials for C. anophelis. Additionally, host preference of midges is one of the critical determinants of vector competence of midge-borne diseases [11,12]. The host preference is largely determined by blood source identification [12-17]. It might be a potential issue for midge blood meal analysis in the circumstances when C. anophelis specimens are present in a midge collection if specimens are not carefully identified, because the blood source of C. anophelis would be derived from the animals that mosquitoes feed on. The significant lack of knowledge about C. anophelis definitely warrants further investigations to increase the understanding of the midge.

Table 1. Mosquito species known to be infested by C. anophelis

Ethical approval

The study was carried out with the full approval of cow keepers and sampling was undertaken with approval of Yanfeng County, Haikou City, Hainan Province, China.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

All authors made contribution to the collection of insects. YM, JX and ZY discussed the paper structure, and JX and YM wrote the manuscript. HS edited the video. All authors read and approved the final version of the manuscript.

Acknowledgments

We thank Professor Yixin Yu in Center for Disease Control and Prevention of PLA for his confirmation of identification of the midge Culicoides anophelis. YM was supported by a grant of National Natural Science Foundation of China-Yunnan Joint Fund (U0932604), JX was supported by a NIH grant (1SC2GM092789-01A1).

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