Journal of Kasetsart Veterinarians vol. 28 No. 2. 2018 วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ Host preference of mosquitoes in an area with high transmission rate of of Kandal province, ความชอบโฮสท์ของยุงชนิด Culex ในพื้นที่ที่มีการถ่ายทอด โรคไข้สมองอักเสบสงในเขตจังหวัดู Kandal ประเทศกัมพชาู

Kshitiz Shrestha1,2, Sebastien Boyer2, Veronique Chevalier,3,4 and Chalalai Rueanghiran1,* Kshitiz Shrestha1,2 Sebastien Boyer2 Veronique Chevalier3,4, และ ชลาลัย เรืองหิรัญ1,*

1Faculty of Veterinary Medicine, Kasetsart University, Bangkok 10900, 1คณะสัตวแพทยศาสตร์ มหาวิทยาลัยเกษตรศาสตร์ กรุงเทพฯ 10900 2Medical Entomology Platform, Institut Pasteur du Cambodge, Phnom Penh, Cambodia. 3CIRAD-Bios, UMR ASTRE, Montpellier, France 4Institut Pasteur du Cambodge, Epidemiology and Public Health Unit, Phnom Penh, Cambodia *Corresponding author: [email protected]

บทคัดย่อ

ยุงเป็นพาหะน�ำโรคหลายชนิด การเกิดโรคที่น�ำโดยยุงนั้น มีปัจจัยเกี่ยวข้องกับชนิดของโฮสท์ ที่ยุงแต่ละชนิดชอบ การระบุชนิดของโฮสท์ที่ยุงแต่ละชนิดชอบนั้น นิยมใช้มุ้งตาข่ายร่วมกับเหยื่อล่อ ในการเก็บตัวอย่าง จุดประสงค์ของการศึกษานี้ เพื่อศึกษาพฤติกรรมการเลือกกินของยุงในจังหวัด Kandal ประเทศกัมพูชา โดยใช้มุ้งชนิด Double net ร่วมกับเหยื่อ 5 ชนิด ได้แก่ โค ไก่ สุกร คน และมุ้งที่ ไม่ใส่เหยื่อ โดยท�ำการทดสอบทั้งหมด 5 วันติดต่อกัน ร่วมกับการหมุนต�ำแหน่งชนิดของเหยื่อ ซึ่งในหนึ่งคืน จะท�ำการเก็บตัวอย่างยุงทั้งหมด 4 รอบ จากการศึกษาพบว่า สามารถดักยุงได้ทั้งหมด 12,573 ตัว จาก ยุง 7 ชนิด โดยชนิดยุงที่พบมากเป็นอันดับต้น ได้แก่ Culex vishnui (36.7 %) Anopheles genus (31.9 %) และ Cx. tritaeniorhynchus (30.4 %) สัดส่วนของยุงที่พบในแต่ละประเภทของเหยื่อล่อ ที่ใช้ดักมีดังนี้ เหยื่อประเภทไก่พบ 12.4 % เหยื่อประเภทโค 49.3 % เหยื่อคน 12.6 % เหยื่อประเภทสุกร 20.2 % และแบบไม่ใส่เหยื่อพบยุง 5.3 % กับดักยุงชนิดที่ใช้โคเป็นเหยื่อจะมีความดึงดูดมากที่สุด เหยื่อที่ เป็นคนจะดึงดูด Cx. quinquefasciatus มากกว่าเหยื่อที่ใช้สัตว์ นอกจากนี้ยังพบยุงชนิดเดียวกัน วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ 127

ในกับดักที่ใช้เหยื่อต่างชนิดกัน ซึ่งบ่งถึงพฤติกรรมการกินแบบ opportunistic behaviour โดยยุงพาหะ ที่มีพฤติกรรมดังกล่าวจะมีโอกาสที่จะรับและแพร่กระจายโรคไวรัสจากสัตว์สู่คนได้ดี ค�ำส�ำคัญ: กับดักตาข่ายสองชั้น กัมพูชา ยุง พฤติกรรมกินอาหาร

ABSTRACT in more than one baited trap which suggested that the mosquitoes have opportunistic Mosquitoes are vector for several behaviour. This suggests have wide disease causing agents. The incidence of opportunity to acquire and transmit viruses mosquito borne diseases is influenced by from to human. mosquito host selection. For the determination Key words: Cambodia, double net trap, of the host preference of mosquito species, mosquitoes, trophic behavior; collection of mosquitoes straight from the baited net can be considered the most INTRODUCTION representative method. The aim of this study was to analyse the feeding behaviour of the Mosquito acquires blood from multiple mosquitoes in Kandal province of Cambodia. hosts such as bird, human, cattle, and other Double nets for five different baits: cow, chicken, vertebrates which increases the risk of pig, human and empty were used to trap transmitting the pathogens among hosts mosquitoes in a rural area of Cambodia for five during blood feeding. Some hosts can be consecutive nights. Every night, the baits with intermediate, while some are permanent the double nets were rotated in the assigned hosts. Mosquito is considered a paramount location. Mosquitoes were collected four vector for its ability to transmit many viruses times a night. In total 12,573 mosquitoes of (Lindahl, 2012). More than 200 arboviruses seven types were captured. Culex vishnui are suspected to be mosquito-borne (DeFoliart (36.7 %) followed by Anopheles genus et al., 1987) out of 500 recognized arboviruses (31.9 %) and Cx. tritaeniorhynchus (30.4 %) to date (Karabatsos, 1985). were the most trapped mosquitoes. The Mosquitoes have developed biting mosquitoes trapped were 12.4 % in chicken, patterns or rhythms with which they feed on 49.3 % in cow, 12.6 % in human, 20.2 % in their hosts. This is an adapted mechanism pig, and 5.3 % in empty trap. Trap-cow was of the mosquitoes that provides them more the more attractive. Cx. quinquefasciatus access to available host. Thus, the biting was more attracted by human than other activity of every vector species has been . Same mosquito species were found found to differ with different hours. Cx. vishnui, 128 วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ and Cx. tritaeniorhynchus were found to be baited double net trap method was more active all night (Chen et al., 2014; Hossain efficient in trapping Aedes albopictus, et al., 2015; Karlekar and Andrew, 2016). Anopheles mosquitoes, and Cx. mosquitoes Studies have reported that the biting activity than other nets during day or night. They of Cx. tritaeniorhynchus peaks toward midnight also showed that mosquito numbers were (Hossain et al., 2015; Reuben, 1971). In contrary, affected by the types of traps used and not a study by Reisen and Aslamkhan (1978) in by location or collection date. found biphasic cycle with dusk and Knowledge of the host preference, dawn peaks. While, a triphasic cycle was biting and resting behaviours of female observed with dusk, midnight, and dawn mosquitoes is important in determining peaks in the (Reisen and and establishing appropriate vector control Aslamkhan, 1976). measures for implementation and also There are several physical, chemical understanding the epidemiology of any and visual factors that come into act to which disease transmitted by mosquitoes. Providing mosquitoes are attracted. The secretions host choices in the field for mosquito vector from the body such as sweat, odour, bacterial species is one scientific approach developed secretions from the host body, flatus are the in order to understand the trophic behaviour host cues (Clements, 1999). The heat and of mosquitoes. Moreover, it allows in moisture released from the body surface of determining the relative abundance and the host determines the attractiveness to the diversity of mosquito species. The feeding mosquitoes (Clements, 1999). The mosquitoes patterns of mosquitoes are dependent have special body feature to detect the on several parameters, particularly two plumes of CO2 released from the host. parameters: an innate characteristic towards Many studies have conducted the host cues, and the relative availability of hosts trapping of mosquitoes using different (Clements, 1992). It is important to understand trapping methods. In the bait studies, various these features of mosquitoes for vector control animals such as chickens, horse, cattle, in order to reduce transmission of arbovirus pigs are used as bait. The human-baited diseases such as Dengue, Chikungunya, double net trap has been used since 1935 Japanese encephalitis (JE), West Nile Virus. and has been quite successful (Gater, 1935; Therefore, the objective of this study was to Le Goff et al., 1997; Rubio-Palis and Curtis, determine the commonly available mosquito 1992; Service, 1977). A study by Tangena species’ trophic preferences in Kandal et al., (2015) demonstrated that the human province, Cambodia. วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ 129 MATERIALS AND METHODS study found a high transmission rate in this area. The study site was located in Kbal In this study, double nets with several Chhroy village, Porti Ban commune, Koh Thom hosts were used to trap mosquitoes during dry district in Kandal province of Cambodia season (March, 2017) in Kbal Chhroy village. (Figure 1). This rural area is located about 60 Specifically built nets called double nets were kilometres from the capital - Phnom Penh city. used to trap mosquitoes. This double net trap It is along the Bassac river and is dominated consisted of an untreated mosquito net, which by agricultural fruits (mango, corn, beans etc.) was raised slightly above the ground to allow and rice cultivation. The immediate vicinity of mosquitoes to enter the trap from its base. the house backyard where traps were placed Another untreated mosquito-net was attached had few human settlements. A small pig farm under the first one. Five different baits were comprising of few hundreds of domestic pigs setup around on an open area at the backyard was located about two hundred meters away of a house for five consecutive nights. In each across the road. A small waste water pond double nets, one cow, one pig, one human, was at the backyard along with few chicken eight chickens were included, but one double houses, an abandoned pig sty, some natural net was without any animal bait as a control. vegetation and fruit trees around. Moreover, Every night, the baits along with their nets were the same area was part of study where rotated among the five assigned location to serological investigation of JE in pig cohorts avoid the bias due to the localisation of were performed (Cappelle et al., 2016). The the double net.

Figure 1 Geographical location of the study site in Cambodia. 130 วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑

Mosquitoes on top of the external collected from cattle net (6,196) followed by net-trap were collected in a paper cup using pigs (2,549), human (1,596), chicken (1,559) mouth aspirator four times a night (2100 hrs, and empty trap (673) as shown in Table 1. midnight, 300 hrs and 600 hrs next morning). Majority of the mosquito species, The collected mosquitoes were identified such as Cx. tritaeniorhynchus, Cx. vishnui, morphologically at Entomological Platform of Anopheles genus mosquito were attracted Institut Pasteur du Cambodge using the to more than one host. Moreover, Anopheles mosquito identification key of Southeast Asian were identified to group level only because nations (Rattanarithikul et al., 2005; Reuben most of them had missing body parts and were et al., 1994; Stojanovich et al., 1966). difficult to identify. Mosquitoes were mostly active during early evening to midnight RESULTS (Figure 2). Most of mosquitoes (38.3 %) were trapped at 9PM, followed by midnight Out of total 12,573 mosquitoes trapped (31.9 %), 3 AM (16.1 %), 6 AM (13.2 %). in double nets, majority of the mosquitoes were

Table 1 Mosquito species and number of mosquitoes collected per traps during the dry season in Kandal province, Cambodia. Species Cx. Cx. Cx. Cx. Anopheles Mansonia Armigeres Total Vishnui Gelidus Tritaeniorhynchus quinquefasciatus genus uniformis subalbatus (N) Bait type Chicken 797 17 315 1 427 0 2 1559 (51.12%) (1.09%) (20.21%) (0.06%) (27.39%) (0.00%) (0.13%) Cow 1606 19 2210 0 2352 6 3 6196 (25.92%) (0.31%) (35.67%) (0.00%) (37.96%) (0.10%) (0.05%) Empty 277 11 198 3 184 0 0 673 (41.16%) (1.63%) (29.42%) (0.45%) (27.34%) (0.00%) (0.00%) Human 955 16 346 11 261 7 0 1596 (59.84%) (1.00%) (21.68%) (0.69%) (16.35%) (0.44%) (0.00%) Pig 969 26 753 4 782 12 3 2549 (38.01%) (1.02%) (29.54%) (0.16%) (30.68%) (0.47%) (0.12%) All baits 4604 89 3822 19 4006 25 8 12573 (36.62%) (0.71%) (30.40%) (0.15%) (31.86%) (0.20%) (0.06%) วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ 131

Figure 2 Periods of Host seeking activity of Cx. vishnui , Cx. tritaeniorhynchus, and Anopheles

DISCUSSION a high percentage of Cx. quinquefasciatus feeding on rabbits. Overall, it might be The study showed that various concluded that these mosquitoes are mosquitoes are attracted to different hosts, opportunistic feeder and could feed on particularly, the cattle. Human or animals are wide variety of hosts. This conclusion not equally attracted by mosquito species was consistent with our study which found (Mukabana et al., 2002). In our study, Cx. Cx. quinquefasciatus in all baited-traps. quinquefasciatus showed an important Cx. tritaeniorhynchus and Cx. vishnui served attraction for both pigs and humans. Cx. as the major dominant species trapped in quinquefasciatus is known to be vector of this study. They are known to be major vector zoonotic diseases such as lymphatic of JE, and are zoophilic and feed largely on filariasis, Western equine encephalitis, both ruminants and pigs (Colless, 1959; West Nile fever, Zika virus infection. Though Longbottom et al., 2017). It was surprising Cx. quinquefasciatus mosquitoes is highly that Cx. tritaeniorhynchus which was the anthropophilic (Lindahl, 2012), they were not main JE vector for the transmission of virus always attracted by humans. Some reports from the amplifying host (pig) in Southeast suggested that Cx. quinquefasciatus had Asia was found more in cattle trap than pig outstanding ornithophilic behaviour as well trap in our study. Nevertheless, this finding (Humeres et al., 1998; Stein et al., 2013). was similar to the findings by Lindahl (2012). A finding by Stein et al. (2013) reported Another entomological study by Lord et al., 132 วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑

(2016) gave evidence that trapping of Cx. However, in this study, in order to reduce tritaeniorhynchus was higher from households the possibility of mosquito escaping the net, with cattle compared to households without the collection of mosquitoes was conducted cattle or from any resting sites. These findings every three hours. suggested that Cx. tritaeniorhynchus preferred Multiple feeding possibilities for vectors cattle to pigs. have been recognized (Edman and Downe, Literature suggested that Cx. gelidus 1964). Triple feeding by Cx. tritaeniorhynchus showed strong preference for feeding on and Ma. uniformis on cows, humans and cattle (Reuben et al., 1992). This species pigs has been reported (Samuel et al., 2008). were known to be positively associated with In our study, engorged mosquitoes were presence of cattle (Hasegawa et al., 2008). also trapped which indicates the possibility However, in our study, Cx. gelidus was not of multiple feeding behaviour (searching trapped in many numbers in cattle trap and behavior for another host in blood-fed other animal traps. Possibly, the Cx. gelidus mosquitoes). Multiple-feeding behaviour were not high in population at the study areas. in mosquitoes should be considered in In a study in Cambodia, cow-baited future study for the possibilities of disease tents were used and were found highly transmission. effective in sampling Anopheles malaria Using the baited hosts is cost-effective vectors (Laurent et al., 2016). The same method to study the trophic behaviour of study also showed that the Anopheles are mosquito vectors as a variety of hosts are attracted by cows and are highly effective in placed in a reachable site for the mosquito reducing human exposure to the Anopheles. vectors. The vectors are attracted in natural The double net may underestimate the way to their hosts. This shows their preferences true mosquito abundance that may escape towards the respective hosts. However, the net when they cannot feed (Kilama et al., mosquitoes that flew into the net trap either 2014; Le Goff et al., 1997; Rubio-Palis and for resting or some other purpose cannot be Curtis, 1992; Service, 1977). There are several understood through this method. Another records of varying amount of success gained limitation of this study was the data obtained using this kind of traps (Le Goff et al., 1997; from only one experiment in one site conducted Rubio-Palis and Curtis, 1992; Service, 1977). during dry season, and mosquitoes appeared They have shown that there are not high to less abundant during the dry or hot seasons differences in the mosquito catches with than the wet season (Sungvornyothin et al., double net or human landing catches. 2009). Some mosquitoes can escape while วารสารสัตวแพทย์ ปีที่ ๒๘ ฉบับที่ ๒ ๒๕๖๑ 133 a person entered inside the net to collect around cattle at dusk (Reuben et al., 1992). the mosquitoes. Other mechanisms such as These are the hours when humans usually body size, body temperature, amount of CO2 come back to rest in or around their house. emission effecting on vector attraction (Port This indicates that sleeping under a mosquito et al., 1980) were not completely accurate net is not enough to protect humans from JE. among the different baits used. The trophic behaviour of mosquitoes during The height of the animal such as cow the day time is to be studied to understand and chicken are another two distinctly different their activity during the day. to host attraction factors. The height from the ground (height of animals) at which hosts are CONCLUSIONS exhaling might play role in attracting different number of mosquitoes (Takken and Verhulst, The mosquitoes are attracted to cattle 2013). The overall mosquitoes were found to and other animals more than humans. This be active during early dusk to midnight and mosquito trapping method (using nets) gradually declined their activity. When the nets helps to keep the bait (animal) safe from were setup from 6 pm, this hindered the mosquito biting and which is in accordance possibility to catch those mosquitoes which to the animal welfare perspective. At the were active during early dusk or daytime. This same time, the mosquitoes can be diverted can be the reason why Aedes mosquito from humans to animals. Since, mosquitoes species were not trapped in this study are attracted to cattle a lot, placing a cattle because they are usually active at daytime. nearby a human house can be an option Also, it has been reported that Aedes theoretically in reducing human exposure to species are trapped more using traps like the vectors and keeping the human safe from BG-Sentinel (Roiz et al., 2016) but light traps the biting mosquitoes. were not found to be successful for trapping There are indeed several factors to Aedes species (Lindahl, 2012; Sriwichai et al., consider for the trophic behaviour study of 2015). mosquitoes and are not that easy to take into On the other hand, Cx. tritaeniorhynchus account each of them. The mosquitoes can was found to be more active from 6 pm to be opportunistic feeder and do not really midnight. Studies have reported the frequent stick with one host. 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