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Migratory Birds As Disseminators of Ticks and the Tick-Borne Pathogens Borrelia Bacteria and Tick-Borne Encephalitis

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Migratory Birds As Disseminators of Ticks and the Tick-Borne Pathogens Borrelia Bacteria and Tick-Borne Encephalitis Wilhelmsson et al. Parasites Vectors (2020) 13:607 https://doi.org/10.1186/s13071-020-04493-5 Parasites & Vectors RESEARCH Open Access Migratory birds as disseminators of ticks and the tick-borne pathogens Borrelia bacteria and tick-borne encephalitis (TBE) virus: a seasonal study at Ottenby Bird Observatory in South-eastern Sweden Peter Wilhelmsson1,2*, Thomas G. T. Jaenson3, Björn Olsen4, Jonas Waldenström5 and Per‑Eric Lindgren1,2 Abstract Background: Birds can act as reservoirs of tick‑borne pathogens and can also disperse pathogen‑containing ticks to both nearby and remote localities. The aims of this study were to estimate tick infestation patterns on migratory birds and the prevalence of diferent Borrelia species and tick‑borne encephalitis virus (TBEV) in ticks removed from birds in south‑eastern Sweden. Methods: Ticks were collected from resident and migratory birds captured at the Ottenby Bird Observatory, Öland, Sweden, from March to November 2009. Ticks were molecularly identifed to species, and morphologically to devel‑ opmental stage, and the presence of Borrelia bacteria and TBEV was determined by quantitative real‑time PCR. Results: A total of 1339 ticks in the genera Haemaphysalis, Hyalomma, and Ixodes was recorded of which I. ricinus was the most abundant species. Important tick hosts were the European robin (Erithacus rubecula), Blackbird (Turdus merula), Tree pipit (Anthus trivialis), Eurasian wren (Troglodytes troglodytes), Common redstart (Phoenicurus phoenicurus), Willow warbler (Phylloscopus trochilus), and Common whitethroat (Sylvia communis). Borrelia bacteria were detected in 25% (285/1,124) of the detached ticks available for analysis. Seven Borrelia species (B. afzelii, B. burgdorferi (s.s.), B. garinii, B. lusitaniae, B. turdi, B. valaisiana, and B. miyamotoi) were identifed. B. turdi was recorded for the frst time in ticks in Sweden. The number of Bor- relia cells per tick ranged from 2.0 100 to 7.0 105. B. miyamotoi‑containing ticks contained a signifcantly higher median number of Borrelia cells than B. burgdorferi× (s.l.)‑×containing ticks. B. garinii and B. miyamotoi were the most prevalent Borrelia species in tick larvae. Larvae of I. ricinus with B. garinii were removed from seven bird species, particularly S. communis and A. trivialis, which may suggest that the larvae had contracted the Borrelia bacteria from or via these birds. Also, a high percent‑ age of tick larvae containing B. miyamotoi was removed from E. rubecula. All ticks were negative for TBEV. Conclusions: The results corroborate the view that the contributions of birds to human disease are substantial, par‑ ticularly as blood hosts for ticks and for their short‑, medium‑, and long‑distance dispersal. Moreover, several ground‑ foraging bird species appear to be important for the maintenance and dispersal of Borrelia species. The absence of TBEV in the ticks conforms to other similar studies. *Correspondence: [email protected] 1 Division of Infammation and Infection, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden Full list of author information is available at the end of the article © The Author(s) 2020. 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://crea‑ tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo‑ main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wilhelmsson et al. Parasites Vectors (2020) 13:607 Page 2 of 17 Keywords: Migratory birds, Borrelia prevalence, Borrelia burgdorferi (sensu lato), Borrelia miyamotoi, Tick‑borne encephalitis virus Background spring, and early summer migration and from Sweden Several species of ticks are known to infest birds, and during their southward, late summer and autumn migra- such birds can disperse ticks over short, medium and tion. In particular, the present investigation was designed long distances [1]. Certain potentially human-pathogenic to determine the abundance of diferent tick species and microorganisms are vectored by ticks. Some of these tick stages infesting migratory and other birds captured microorganisms may be harboured in both ticks and at one of Sweden’s most important bird observatories. birds. Obviously, microorganism-containing vector-com- Moreover, we aimed at determining the prevalence of petent ticks, while feeding on a susceptible avian host, Borrelia and TBEV contents in the ticks infesting the can transmit the microorganism to its host. Certainly, birds. transmission of a blood-borne microorganism can also take place in the opposite direction, whereby infectious, Methods transmission-competent birds (transmission hosts or res- Description of the sampling site, Ottenby Bird Observatory ervoir-competent hosts) can infect feeding, susceptible Ottenby Bird Observatory is located on the southern ticks. During their fights birds can act as “vehicles” for point of the island of Öland in south-east Sweden. At the geographic spread of diferent types of human-patho- the observatory, migratory birds have been banded since genic microorganisms, i.e. for microorganisms which are 1946, and more than 1 million birds have been caught, maintained in both birds and ticks, for microorganisms providing a solid knowledge base on which bird popula- mainly or only present in ticks, and for microorganisms tions that pass through the area [23, 24]. Apart from fun- mainly or only present in birds. Tick-associated micro- nelling migratory birds during migration, the area also organisms, with proven, suspected, or unknown human functions as stopover site and breeding ground for many pathogenicity which have been detected in bird-infesting species of birds. In spring, the vast majority of birds ticks in Europe include Borrelia afzelii [2–5], Borrelia caught at the observatory have just arrived after a night burgdorferi (s.s) [2, 4, 6, 7], Borrelia garinii [2–5, 7, 8], of migration, including passage over stretches of open Borrelia lusitaniae [9], Borrelia turdi [3, 5, 10–12], Bor- water (the Baltic Sea), while in autumn, birds caught will relia valaisiana [2–4, 10, 11, 13], Borrelia spielmanii [4, be a mixture of birds arriving from areas to the north 5], Borrelia miyamotoi [2, 4, 14], Neoehrlichia mikuren- and east, and those that have spent some time on stopo- sis [4, 14–16], Rickettsia aeschlimannii [16, 17], Rickettsia ver in the area and restarting migration. Te reserve in africae [17], Rickettsia helvetica [14, 16, 18, 19], Rickett- which the observatory is situated encompasses an area sia japonica [16], Rickettsia monacensis [16], Anaplasma of about 25 km2 with shore meadows, pastures, and phagocytophilum [14, 19], Babesia venatorum [16], Babe- woodland dominated by stands of old oaks (Quercus sia microti [16], tick-borne encephalitis virus (TBEV) [16, robur) and birch (Betula sp.). Te area is grazed by cattle 20], Alkhurma haemorrhagic fever virus (AHFV) [21], (Bos taurus), sheep (Ovis aries) and fallow deer (Dama and Crimean-Congo haemorrhagic fever virus (CCHFV) dama). [22]. Seasonal migration is common among birds breeding Bird captures and tick collections in northern latitudes but shows large variation between Sampling of birds was approved by the Swedish Board and within species in timing and direction of migration of Agriculture, delegated through the Animal Research as well as distance travelled. Most migratory birds divide Ethics Committee in Linköping (decision 43–09). Birds the trip into several migration legs, interspersed with were captured during the general trapping activities of time spent on stopover sites along the route. At suit- staf members at the Ottenby Bird Observatory (56° 12′ able stopover sites, birds feed and prepare for the next N, 16° 24′ E). With the approval of the Swedish Museum leg of migration, providing opportunities for new ticks of Natural History in Stockholm, Sweden, mist nets and to attach and already fed ticks to detach from the birds, Heligoland traps were used to capture birds during the thereby following birds along the migratory routes and periods 15 March–15 June and 15 July–15 November potentially creating new foci of tick-borne diseases. 2009 as part of the observatory’s standardized trapping Te overall aim of this study is to better understand the scheme. Trapped birds were banded, measured, and potential role of birds as disseminators of ticks and tick- identifed to species level and, when possible, sexed and borne pathogens into Sweden during their northward, aged. At the observatory, trapping starts half an hour Wilhelmsson et al. Parasites Vectors (2020) 13:607 Page 3 of 17 before sunrise and ends at 11 a.m., which means that Total nucleic acid extraction and cDNA synthesis from ticks the length
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