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Background Zoological gardens contain unique configurations 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 interspecific 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 different trapping methods. Blood-fed mosquitoes were identified and their blood meal was amplified by PCR, sequenced, and blasted for host species identification. Results In total, 640 blood-fed mosquitoes were collected [Culex pipiens (n = 497), Culiseta annulata (n = 81), Anopheles maculipennis s.l. (n = 7), An. claviger (n = 1), and unidentifiable (n = 55)]. Successful identification of the host species 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 efficient 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 significantly associated with the proportion of captured blood-fed mosquitoes by generalized linear modelling. Conclusions Mosquito feeding behaviour in zoos is mainly influenced by time, location (sampling area), temperature, 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. Graphical Abstract

Background Avian malaria has caused mortalities in captive penguins worldwide and it is a conservation threat for some wild penguins. The experience of staff working on penguins is highly valuable for the improvement of captivity conditions. Methods An online questionnaire was designed to collect avian malaria information in penguins in the UK. Volunteers with diverse experience reviewed it for scientific value and clarity, and it was supported by the British and Irish Association of Zoos and Aquariums. Results Forty-two institutions were contacted by email, obtaining 27 complete and five partial responses. Eighteen institutions reported avian malaria in 38 suspected and 37 confirmed outbreaks in the past 20 years, mainly occurring in the summer and recent years. Proportional risk was higher in the south east region of England. Humboldt and African penguins were more commonly affected, and prevalence was mostly low or medium, but lethality was high. Different treatment protocols were reported with inconsistent outcomes. Conclusions Penguins' susceptibility, their translocation across institutions, and the wide distribution of avian malaria make this disease a constant threat. Preventive and control measures are recommended, including testing for early diagnosis and treatment, avoiding prolonged stressful events in penguins, and monitoring and controlling mosquito vectors.

Additional file1: Table S1. Variables and values considered for the environmental analysis. Table S2. Values of the categorical variables for each trap. Table S3. Host choices of blood-fed mosquitoes captured in Chester Zoo, 2017. Table S4. Host choices of blood-fed mosquitoes captured in Chester Zoo, 2018. Table S5. Host choices of blood-fed mosquitoes captured in Chester Zoo, 2019. Table S6. Host choices of blood-fed mosquitoes captured in Flamingo Land, 2017. Table S7. Values of the generalised linear models for the significant variables in relation to the capture of blood-fed mosquitoes. Figure S1. Host patterns of blood-fed mosquitoes. Birds in shades of blue, non-human mammals in shades of red. Zoo vertebrates are indicated with an asterisk.

Background: Zoological gardens contain unique configurations 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 interspecific pathogen transmission risks involving zoo animals, like avian malaria to captive penguins. Understanding mosquito ecology and host preferences is necessary to improve mosquito control and disease prevention measures in these environments. Methods: Mosquito sampling took place in Chester Zoo for three years (2017 to 2019) and for one year in Flamingo Land (2017) using different trapping methods. Blood-fed mosquitoes were identified and their bloodmeal was amplified by PCR, sequenced, and blasted for host species identification.Results: In total, 640 blood-fed mosquitoes were collected (Culex pipiens (n = 497), Culiseta annulata (n = 81), Anopheles maculipennis s.l. (n = 7), An. claviger (n = 1) and unidentifiable (n = 55)). Successful identification of the host species was achieved from 159 of the 640 blood-fed mosquitoes. Mosquitoes fed on birds (n = 74), non-human mammals (n = 20) and humans (n = 71). There were mixed bloodmeals 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 efficient techniques for capturing blood-fed mosquitoes than traps for host-seeking or gravid mosquitoes. By relating the locations of zoo animals to where fed mosquitoes were trapped, the minimum travelling distances were calculated (13.7 to 366.7 meters). Temperature, precipitation, relative humidity, proximity to zoo animal exhibits and vegetation level were found to be significantly associated with the proportion of captured blood-fed mosquitoes by generalized linear modelling.Conclusions: Mosquito feeding behaviour in zoos is influenced by environmental variables 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 animals.

Avian malaria is one of the most serious diseases in penguins under human care and could become a severe threat to the conservation of vulnerable wild populations. It is caused by the Haemosporidia parasites of the genus Plasmodium and needs a mosquito vector for its transmission. We captured mosquitoes during two years in Chester Zoo (Cheshire) and one year in Flamingo Land (Yorkshire); both zoos house Humboldt penguins (Spheniscus humboldti). The mosquito temporal and spatial abundance across the seasons and sites were analysed. It was found that Culex pipiens, the principal avian malaria vector in Europe, was the most abundant species. There was a peak in the mosquito abundance during the summer as expected, but it was at different months between sites and years. The abundance of mosquitoes also varied among sampling areas; one area in Chester Zoo captured a greater proportion of mosquitoes than the others in both years, and in Flamingo Land, we also found an area with consistent high catches. Blood-fed mosquitoes were captured and analysed to identify the host on which they had fed. Different proportions of blood-fed mosquitoes were captured by areas and months; more were collected during the summer and in certain areas that not in all cases were related to a high abundance of un-fed mosquitoes. Most of these mosquitoes were Culex pipiens and Culiseta annulata; it was confirmed that the first one prefers to feed on birds and the second one on non-human mammals. However, many Culex pipiens fed on humans, which alert us about the possible nuisance for visitors and the potential transmission risk of zoonotic diseases. A partially identified Culicinae mosquito, likely to be Culex pipiens, and an Anopheles maculipennis s. l. fed on penguins; so, they could be involved in avian malaria transmission. It was found that mosquitoes travel variable distance after feeding and therefore, the control measures against mosquitoes should cover more than the areas of immediate concern. The environmental variables were analysed to understand the drivers of the diverse mosquito captures. The temperature was the most important variable related to mosquito abundance, and the dense vegetation, proximity to mosquito oviposition sites and closeness to animal exhibits were also significant. Therefore, the temperature could guide actions for mosquito control and avian malaria prevention and avoiding those surrounding features near the penguin exhibits could prevent high densities of mosquitoes. Many aspects of avian malaria epidemiology are uncertain so, through an online survey, the knowledge of the staff in zoos and wildlife parks about the disease was gathered. It was found that avian malaria had affected penguins in more than half of the answering institutions, involving mainly Humboldt and African penguins (Spheniscus demersus) with high lethality rates; therefore, efforts on preventive actions are encouraged. Avian malaria parasites were found in Culex pipiens mosquitoes and their saliva, wild birds and penguins, suggesting that the transmission process happens locally. Mosquito populations are dynamic, and the biosurveillance of their populations is needed to better understand their role as disease vectors and to implement effective control measures at the right time, assisting in this way the prevention of avian malaria in captive penguins.

Los humedales son de los ecosistemas más importantes en el mundo por la gran diversidad biológica que albergan y los recursos y servicios ecosistémicos que proporcionan; sin embargo, su conservación está severamente amenazada. Las aves acuáticas son uno de los componentes más representativos de la biodiversidad de los humedales y es necesario estudiar sus comunidades para establecer prioridades de protección adecuadamente. En este estudio describimos la riqueza de especies y abundancia relativa de la comunidad de aves acuáticas de un humedal del Estado de México que visitamos desde agosto de 2010 al mes de agosto de 2011. Encontramos 23 especies de aves acuáticas, la mayoría pertenecen a las familias Anatidae (patos) y Ardeidae (garzas) y registramos una abundancia acumulada de 25,220 individuos. Realizamos una curva de acumulación de especies y empleamos el modelo de Clench, cuya estimación fue de 24 especies; por lo tanto, observamos al 95% de las especies predichas. La lle­gada de especies migratorias contribuyó evidentemente al incremento de la riqueza de especies y la abundancia de individuos, especialmente de octubre a marzo. Consideramos que la riqueza de especies y la abundancia que registramos, así como la observación de especies poco comunes, especies reproduciéndose y especies sujetas a una categoría de conservación, indican el gran valor ecológico de este humedal a pesar de su extensión limitada. Por lo tanto, es relevante evaluar las características ecológicas de los humedales naturales y artificiales, incluyendo a las comunidades de aves acuáticas, para mejorar las acciones de conservación en esta región.