Diversity, ecology and vector potential of mosquito populations (Diptera: Culicidae) in two differentially structured zoological gardens in Germany

The present work focusses on the mosquito populations of two zoological gardens in Germany with the aim to better understand mosquito biology of native species and to contribute to a greater awareness of mosquito and mosquito-borne disease agent surveillance in zoos. For this purpose, data on species composition, blood meal patterns and mosquito-borne pathogens were analysed. The investigated zoological gardens differed not only in their sizes and animal stocks, but also in their surrounding environments. The 160 ha Tierpark Berlin is located in a densely populated urban area, while the 15 ha Zoological Garden Eberswalde is surrounded by forest. To gain an overview about the mosquito fauna of both zoos, adult specimens were caught by aspirating and EVS-trapping during the 2016 season. In addition, larval stages were collected from their breeding sites located in the zoo areas. In total, 2,257 mosquitoes were sampled, belonging to 20 taxa. Seasonal differences between the zoos were documented, both in terms of species composition and the relative abundance of mosquito species collected. As the studied zoos were located in the same climatic region and both locations provided similar breeding sites, differences in species composition were attributed to the entry of mosquitoes from surrounding landscapes. Influencing factors could have been the different sizes of the zoos and variations in the potential host animal populations. According to the vector potential of most frequently collected taxa in the Zoological Garden Eberswalde (Annulipes Group, Culiseta annulata), TAHV, USUV, WNV, filariae and avian malaria parasites appear to have the highest risk of being transmitted at this location. In the Tierpark Berlin, Aedes vexans was the most frequently collected mosquito species, suggesting a theoretical risk for the transmission of a broader spectrum of pathogens due to covered vector competences. Pathogens such as BATV, SINV, TAHV, USUV and filarial worms could be of major importance regarding transmission risk to zoo animals, as they had previously been found to circulate Germany. In addition, avian malaria parasites represent a considerable risk for susceptible exotic bird species in Berlin. Since the blood-feeding behaviour of vector-competent mosquito species has a major influence on the transmission of a mosquito-associated pathogen, the analysis of blood meal patterns is crucial to better understand vector-pathogen cycles. Therefore, blood meals of blood-fed mosquitoes caught in 2016 and 2017 by aspirating and EVS-trapping in the Tierpark Berlin and the Zoological Garden Eberswalde were analysed. The aim was to investigate to what extent native mosquito species accept exotic zoo animals, wild native animals and humans as blood hosts. In addition, it was examined whether the collected species are generalists or specialists when selecting vertebrates for blood feeding. A total of 405 blood-fed mosquitoes from 16 taxa were collected. The genetic analysis of blood meals identified 56 host species, which – in addition to humans – mainly originated from mammals of the zoo animal populations. In agreement with the previous study on the mosquito fauna of the Tierpark Berlin and the Zoological Garden Eberswalde, the analysis of blood meals also showed differences between the two zoos. In the smaller Zoological Garden Eberswalde, a higher number of blood-fed mosquitoes was collected than in the Tierpark Berlin, probably caused by a higher host density in Eberswalde, which may have led to an overall higher mosquito density. However, no differences between both zoos were observed with respect to the blood feeding behaviour of the analysed mosquito species: Mosquitoes of both locations were rather generalistic, although species could be grouped according their blood meals into 'amphibian', 'non-human mammal' and, ‘non-human mammal and human' feeding species. The more random selection of hosts could indicate a low probability of effective pathogen transmission by applying the 'dilution effect'. Notwithstanding, since wild animals have also been accepted as hosts, pathogen transmission by bridge vectors from one vertebrate group to another could be relevant in the sampled zoos. Adult mosquito specimens collected in 2016 and 2017 were screened for filarial nematodes, avian Haemosporidia and mosquito-borne viruses. Dirofilaria repens was detected in a mosquito from the Zoological Garden Eberswalde. Mosquitoes from Berlin and Eberswalde were tested positive for the nematode species S. tundra. Sindbis virus was found in a mosquito pool collected in the Tierpark Berlin, while no mosquito-associated viruses were detected in specimens collected in the Zoological Garden Eberswalde. Mosquitoes from both zoos were positive for the haemosporidian parasites Haemoproteus sp. and Leucocytozoon sp., and one documentation was made for avian Plasmodium sp. in the Tierpark Berlin. The identified pathogens have the potential to cause disease in captive and wild animals, and some of them also in humans. Most of the mosquitoes tested positive had been collected in July, suggesting a high infection risk during this month. Since most pathogen detections were made from species belonging to the Cx. pipiens complex, species of this complex seem to be most relevant in the studied zoos when it comes to mosquito-borne pathogen transmission. Although mosquitoes are no proven vectors of most of the avian malaria parasite genera found, evidence for Haemoproteus sp. and Leucozytozoon sp. demonstrated a high prevalence of avian malaria parasites in the zoos. In summary, the results of the three studies indicate regional differences both in the mosquito species composition and in the occurrence of mosquito-borne pathogens. However, no differences were found between the mosquito communities of both zoos concerning their blood feeding behaviour, suggesting that the general behaviour of the insects is location-independent. Several potential disease agents were found in the collected mosquitoes, although not at high abundances. Whether these pathogens were found by chance in the two zoos or whether the particular zoo environment is a hot spot of arthropod-borne pathogens cannot be determined with the studies conducted. Nonetheless, it seems clear that zoological gardens are attractive to mosquito females not only in their search for breeding sites, but also when looking for blood hosts and places for mating or resting. These advantageous conditions also attract mosquito species that have their larval habitats outside the zoological gardens, which is why elimination of breeding sites on the zoo premises alone will not necessarily keep away all mosquitoes. A closer collaboration between zoological gardens and entomologists could be beneficial for both. Zoo officials could benefit from being able to identify potential arthropod vectors on the zoo grounds and receiving information on circulating arthropod-borne disease agents, as well as on the animal species susceptible to those. For entomologists, zoological gardens are ideal research locations, as they provide an environment with a high diversity of habitats and potential blood hosts for haematophagous arthropods in a confined space. Studying mosquito biology will become even more significant in the future, since in a world that is getting smaller, both potential vectors and pathogens are regularly introduced into areas where they did not occur before. Therefore, it would be desirable if more studies targeting ecological as well as infectiological aspects of vector species in zoological gardens in Germany were carried out.

Die vorliegende Arbeit hat sich mit den Stechmücken Populationen zweier Zoologischer Gärten in Deutschland befasst. Ziel war es, anhand von Daten über die Arten-Zusammensetzung, den Blutmahlzeiten und über bereits nachzuweisende Stechmücken-assoziierte Pathogene das Vektor-Potential einheimischer Stechmücken besser einzuschätzen und hierbei auch auf regionale Unterschiede einzugehen. Um eine Übersicht über die Stechmückenfauna beider Zoos zu gewinnen, wurden in der Saison 2016 adulte Stechmücken mittels EVS-Fallen und Aspirator gefangen und larvale Stadien aus ihren Brutstätten innerhalb der Zoogelände gesammelt. Insgesamt wurden 2.257 Stechmücken erfasst, die 20 Taxa zuzuordnen waren. Es traten saisonal variierende Unterschiede zwischen Zoos auf, sowohl die Artzusammensetzung betreffend, als auch die relativen Häufigkeiten der gesammelten Stechmücken-Arten. Da das hämatophage Verhalten vektorkompetenter Stechmückenarten essenziell ist für die Übertragung eines Stechmücken-assoziierten Krankheitserregers, ist die Analyse von Blutmahlzeiten entscheidend um Vektor-Pathogen Zyklen besser zu verstehen. Aus diesem Grund wurden die Blutmahlzeiten von Stechmücken analysiert, die in den Jahren 2016 und 2017 mittels EVS-Falle und Aspirator im Tierpark Berlin und Zoologischen Garten Eberswalde gefangen worden sind. Insgesamt wurden 405 blutgesogene Stechmücken aus 16 Taxa gesammelt. Die genetische Analyse der Blutmahlzeiten identifizierte 56 Wirtsarten, die neben einem großen Anteil an Menschen hauptsächlich aus Säugetieren der Zootierpopulationen stammten. An beiden Zoos wiesen die Stechmückenarten ein generalistisches Verhalten bei der Auswahl ihrer Blutwirte auf, wobei die Arten entsprechend ihrer Blutmahlzeiten in ‚Amphibien‘, ,nicht-menschliche Säugetiere‘ und ‚nicht-menschliche Säugetiere und Menschen‘ stechende Arten gruppiert werden konnten. Das eher zufällige Verhalten bei der Auswahl von Wirten deutet bei der Anwendung des ‚Verdünnungseffektes‘ auf eine geringe Wahrscheinlichkeit einer effektiven Erreger Übertragung in einem der beiden Zoos hin. Da aber auch Wildtiere als Blutwirte akzeptiert worden sind, könnten bei einer Übertragung besonders Brückenvektoren eine Rolle spielen, die Pathogene von einer Tiergruppe auf die andere übertragen. Die gesammelten adulten Stechmücken wurden auf Filarien, Haemosporidien und Stechmücken-assoziierte Viren getestet. Hierbei wurde Dirofilaria repens in einer Stechmücke aus dem Zoologischen Garten Eberswalde nachgewiesen. Stechmücken aus Berlin und Eberswalde wurden positiv getestet auf die Nematoden Art Setaria tundra. Sindbis Virus wurde in einem Stechmücken-Pool aus dem Tierpark Berlin gefunden, während kein Stechmücken-assoziiertes Virus aus den in Eberswalde gesammelten Stechmücken nachzuweisen war. Stechmücken aus beiden Zoos waren positiv für die Haemosporidien Haemoproteus sp. und Leucozytozoon sp., während Plasmodium sp. nur in Berlin gefunden wurde. Da die meisten Erreger-Nachweise von Arten des Culex pipiens Komplexes stammten, scheinen diese die relevantesten Vektoren in den untersuchten Zoos zu sein. Alle drei Studien haben gezeigt, dass Zoologische Gärten nicht nur attraktiv sind für Stechmücken, die Eier ablegen, sondern auch für Adulte, die auf der Suche nach Blutwirten, Weibchen zur Paarung oder Ruheplätzen sind. Dadurch werden auch Arten angezogen, die ihre Bruthabitate außerhalb der Zoologischen Gärten haben, weshalb allein eine Überwachung von Bruthabitaten auf dem Zoogelände nicht alle Stechmücken fernhalten kann. Eine engere Zusammenarbeit zwischen Zoologischen Gärten und Entomologen kann vorteilhaft für beide sein. Zoos könnten davon profitieren, potenzielle Vektoren auf dem Gelände zu kennen und eine Übersicht zu haben über zirkulierende Erreger und über die Tierarten, die verwundbar für eventuell schon vorkommende Krankheitserreger sind. Für Entomologen sind Zoologische Gärten ein idealer Forschungsstandort, da sie für Stechmücken eine Vielzahl an Lebensräumen bieten mit einer permanenten Verfügbarkeit von Blutwirten innerhalb eines kleinen Raums. In Zukunft wird die Erforschung von Stechmücken noch mehr an Bedeutung gewinnen, da in einer immer kleiner werdenden Welt potenzielle Vektoren und Krankheitserreger regelmäßig in Gebiete eingeführt werden, in denen sie vorher nicht heimisch waren. Daher wäre es wünschenswert, wenn weitere Studien zu ökologischen und infektiologischen Aspekten von Vektorarten in zoologischen Gärten in Deutschland durchgeführt werden.



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