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Blood-Feeding Ecology of Mosquitoes in Two Zoological Gardens in The

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Blood-Feeding Ecology of Mosquitoes in Two Zoological Gardens in The Hernandez‑Colina et al. Parasites Vectors (2021) 14:249 https://doi.org/10.1186/s13071‑021‑04735‑0 Parasites & Vectors RESEARCH Open Access Blood‑feeding ecology of mosquitoes in two zoological gardens in the United Kingdom Arturo Hernandez‑Colina1,2* , Merit Gonzalez‑Olvera1,2, Emily Lomax1, Freya Townsend1, Amber Maddox1, Jenny C. Hesson3, Kenneth Sherlock1, Dawn Ward4, Lindsay Eckley2, Mark Vercoe2, Javier Lopez2 and Matthew Baylis1,5 Abstract Background: Zoological gardens contain unique confgurations of exotic and endemic animals and plants that create a diverse range of developing sites and potential sources of blood meals for local mosquitoes. This may imply unusual interspecifc pathogen transmission risks involving zoo vertebrates, like avian malaria to captive penguins. Understanding mosquito ecology and host feeding patterns is necessary to improve mosquito control and disease prevention measures in these environments. Methods: Mosquito sampling took place in Chester Zoo for 3 years (2017, 2018, and 2019) and for 1 year in Flamingo Land (2017) using diferent trapping methods. Blood‑fed mosquitoes were identifed and their blood meal was ampli‑ fed by PCR, sequenced, and blasted for host species identifcation. Results: In total, 640 blood‑fed mosquitoes were collected [Culex pipiens (n 497), Culiseta annulata (n 81), Anoph- eles maculipennis s.l. (n 7), An. claviger (n 1), and unidentifable (n 55)]. Successful= identifcation of the= host spe‑ cies was achieved from= 159 blood‑fed mosquitoes.= Mosquitoes fed on= birds (n 74), non‑human mammals (n 20), and humans (n 71). There were mixed blood meals from two hosts (n 6). The= proportions of blood‑fed mosquitoes= varied across sampling= seasons and sites within the zoos. The use of resting= traps and aspiration of vegetation were more efcient techniques for capturing blood‑fed mosquitoes than traps for host‑seeking or gravid mosquitoes. By relating the locations of zoo vertebrates to where fed mosquitoes were trapped, the minimum travelling distances were calculated (13.7 to 366.7 m). Temperature, precipitation, relative humidity, proximity to zoo vertebrate exhibits, and vegetation level were found to be signifcantly associated with the proportion of captured blood‑fed mosquitoes by generalized linear modelling. Conclusions: Mosquito feeding behaviour in zoos is mainly infuenced by time, location (sampling area), tempera‑ ture, and host availability, which highlights the value of mosquito monitoring in complex settings to plan control strategies and potentially reduce inherent disease transmission risks for humans and threatened zoo vertebrates. Keywords: Blood meal, Culex pipiens, Culiseta annulata, Mosquito control, Mosquito dispersal Background Te importance of mosquito-borne diseases continues to increase as invasive mosquito species and associated *Correspondence: [email protected] pathogens are detected in new habitats. Te distribution 1 Department of Livestock and One Health, Institute of Infection, expansion in southern Europe of the Asian tiger mos- Veterinary & Ecological Sciences, University of Liverpool, Leahurst quito (Aedes albopictus), an efective vector of animal Campus, Chester High Road, Neston, Cheshire CH64 7TE, UK Full list of author information is available at the end of the article and human arboviruses, is just one example [1–3], and © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hernandez‑Colina et al. Parasites Vectors (2021) 14:249 Page 2 of 18 although this mosquito is not yet frmly established in [17–19]. Lastly, exotic pathogens can be introduced and the United Kingdom (UK), it could fnd extensive suit- pose new risks for the health of humans and animals. able habitats in the near future due to climate and envi- For instance, Usutu virus (USUV) has caused mortality ronmental changes [4]. Blood-feeding behaviour and in wild birds (e.g. blackbirds, Turdus merula, and great mosquito population density and longevity are key fac- grey owls, Strix nebulosa) [20] and has been detected in tors that infuence the ability of mosquito populations to birds from zoos in central Europe [21]. Recently, it was spread pathogens (a term known as vectorial capacity) [3, detected in birds in the UK and, although the risk for 5, 6]. Investigating vectorial capacity and its key factors humans is low to moderate, constant monitoring is rec- is critical to understanding disease transmission risks ommended [22, 23]. Terefore, zoos are strategic sites for by vectors and fnding efective control approaches [5]. the surveillance of vector-borne pathogens due to their Nonetheless, studying mosquito blood-feeding behaviour unique setting [13]. is challenging, for three main reasons: (i) After feeding, Te vector potential of a mosquito depends on its phys- mosquitoes seek a safe place for egg production; thus, iological competence (if it can amplify the pathogen), the they are not attracted to commonly used traps, which is physiological competence of the host (if the pathogen refected by their low proportion reported, even if the can be amplifed in the host), and the ecological capac- studies target them (3–10% [7–9]). (ii) Mosquitoes can ity (if the environment supports transmission through disperse long distances when they look for potential enough mosquito–host contact). Mosquito species can hosts (e.g. Aedes vexans migrates to invade new habitats exhibit diverse feeding patterns despite being exposed to [10] and Culex spp. can travel for several kilometres [11]) the same vertebrates in a single location [24]. Tey can and after blood-feeding (e.g. Anopheles coluzzii remains be generalists, feeding on a wide range of vertebrate spe- within 50 m from its blood-host and disperses up to cies or groups, or specialists, preferring a narrow range 250 m after 60 h [12]). (iii) Studying mosquito feeding of hosts [25, 26]. Generalist mosquitoes can facilitate patterns in natural settings is a problem of positive fnd- pathogen transmission among unrelated species, and in ing bias because engorged mosquitoes provide informa- such cases they are known as ‘bridge vectors’ [1, 27–29]. tion about the hosts that they choose but not those that However, the feeding of mosquitoes on hosts that can- they avoid. Consequently, to thoroughly understand not harbour the pathogen may lead to a dilution efect host preferences, techniques for capturing blood-fed in pathogen transmission [14]. In the case of specialized mosquitoes should be improved and information about mosquitoes, changes in the host community structure the abundance and density of potential hosts is needed, could force them to feed on unusual hosts [1], which although in many settings this is not feasible to obtain. could also facilitate interspecifc transmission of patho- Knowing the identity and location of vertebrates in acces- gens. For example, Aedes japonicus that usually feeds on sible environments, like zoological gardens, can therefore mammals (mammalophilic) has been found feeding on be advantageous in the study of mosquito host choices birds in some settings [30]. Likewise, when the mamma- and post-feeding dispersal. lian-biting biotype of Culex pipiens (molestus) and its Te zoo environment poses a risk of interspecifc bird-feeding biotype (pipiens) hybridize, the resulting transmission of pathogens among vertebrate groups that population may present mixed-host preferences and act usually cannot happen in natural environments [13]. In as a bridge vector between birds and people [27]. Tere- zoos, mosquitoes have access to a broad range of hosts fore, both generalist and specialist mosquitoes can func- and breeding sites due to the availability of endemic and tion as bridge vectors, and the combination of vector exotic species of fauna and fora [13]. Mosquitoes col- host preference and host competence determine whether lected at zoos have been found feeding on zoo verte- cross-species transmission occurs and whether a dilu- brates, free wild vertebrates, and humans, and mixed tion or amplifcation efect is observed in relation to host blood meals have been reported [8, 14, 15]. Te rele- diversity [31]. vance of mosquito ecology in zoos can be exemplifed by Te aims of this study were to describe the environ- the outbreak of West Nile virus (WNV), transmitted by mental infuence on feeding ecology, host choice pat- Culex spp. mosquitoes, in the Bronx Zoo/Wildlife Con- terns, and post-feeding dispersal of mosquitoes in two servation Park in relation to the frst outbreak of WNV zoological gardens in the UK. Tis information improves in America in humans [16]. Mosquito-borne diseases can our understanding of mosquito populations in zoos and be also a threat for the health of zoo vertebrates; avian provides insights into potential cross-species pathogen malaria (caused by Plasmodium spp. haemosporidians) transmission risks. Over 2 years, we identifed blood clearly exemplifes this, as it is a major cause of severe meals from mosquitoes captured using traps for host- disease and death for captive penguins worldwide, and seeking mosquitoes and for gravid mosquitoes; tech- mosquito control and surveillance has been encouraged niques for capturing blood-engorged mosquitoes were Hernandez‑Colina et al.
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