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Sand Flies (Diptera: Psychodidae) in Eight Balkan Countries

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Sand Flies (Diptera: Psychodidae) in Eight Balkan Countries Dvorak et al. Parasites Vectors (2020) 13:573 https://doi.org/10.1186/s13071-020-04448-w Parasites & Vectors RESEARCH Open Access Sand fies (Diptera: Psychodidae) in eight Balkan countries: historical review and region-wide entomological survey Vit Dvorak1†, Ozge Erisoz Kasap2†, Vladimir Ivovic3, Ognyan Mikov4, Jovana Stefanovska5, Franjo Martinkovic6, Jasmin Omeragic7, Igor Pajovic8, Devrim Baymak9, Gizem Oguz2, Kristyna Hlavackova1, Marketa Gresova1, Filiz Gunay2, Slavica Vaselek1,10, Nazli Ayhan11,12, Tereza Lestinova1, Aleksandar Cvetkovikj5, Darinka Klaric Soldo7, Ivelina Katerinova13, Simona Tchakarova13, Ayda Yılmaz2, Begum Karaoglu2, Jose Risueno Iranzo14, Perparim Kadriaj15, Enkelejda Velo15, Yusuf Ozbel16, Dusan Petric10, Petr Volf1 and Bulent Alten2* Abstract Background: Sand fies (Diptera: Psychodidae) are medically important vectors of human and veterinary disease- causing agents. Among these, the genus Leishmania (Kinetoplastida: Trypanosomatidae), and phleboviruses are of utmost importance. Despite such signifcance, updated information about sand fy fauna is missing for Balkan countries where both sand fies and autochtonous leishmaniases are historically present and recently re-emerging. Therefore, a review of historical data on sand fy species composition and distribution in the region was followed by a large-scale entomological survey in eight Balkan countries to provide a recent update on local sand fy fauna. Methods: The literature search involved the period 1910–2019. The entomological survey was conducted at 1189 sam- pling stations in eight countries (Bulgaria, Bosnia and Herzegovina, Croatia, Kosovo, Montenegro, North Macedonia, Serbia and Slovenia), covering 49 settlements and 358 sampling sites between June and October in the years 2014 and 2016, accumulating 130 sampling days. We performed a total of 1189 trapping nights at these stations using two types of traps (light and CO2 attraction traps) in each location. Sampling was performed with a minimal duration of 6 (Montenegro) and a maximal of 47 days (Serbia) between 0–1000 m.a.s.l. Collected sand fies were morphologically identifed. Results: In total, 8490 sand fy specimens were collected. Morphological identifcation showed presence of 14 spe- cies belonging to genera Phlebotomus and Sergentomyia. Historical data were critically reviewed and updated with our recent fndings. Six species were identifed in Bosnia and Herzegovina (2 new records), 5 in Montenegro (2 new records), 5 in Croatia (2 new records), 9 in Bulgaria (5 new records), 11 in North Macedonia (1 new record), 10 in Serbia (no new records), 9 in Kosovo (3 new records) and 4 in Slovenia (no new records). Conclusions: This study presents results of the frst integrated sand fy fauna survey of such scale for the Balkan region, providing frst data on sand fy populations for four countries in the study area and presenting new species *Correspondence: [email protected] †Vit Dvorak and Ozge Erisoz Kasap contributed equally to this work 2 Department of Biology, Ecology Section, Faculty of Science, VERG Laboratories, Hacettepe University, Ankara, Turkey 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://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. Dvorak et al. Parasites Vectors (2020) 13:573 Page 2 of 15 records for six countries and updated species lists for all surveyed countries. Our fndings demonstrate presence of proven and suspected vectors of several Leishmania species. Keywords: Phlebotomine, Sand fy, Balkans, Species, Morphology Background survey both for a striking lack of updated and validated Phlebotomine sand fies (Diptera: Psychodidae) are medi- data on sand fy vectors and for its importance for vec- cally important as the vectors of Leishmania spp. and tor/pathogen transmission between western European arboviruses that threaten human and animal health. countries and Anatolia, Caucasus, Middle East countries. Within the subfamily Phlebotominae, over 900 species Te region comprises 13 countries namely Albania, Bos- were described so far, of which at least 100 species of nia and Herzegovina, Bulgaria, Croatia, Greece, Kosovo, the genera Phlebotomus and Lutzomyia are suspected or Moldova, Montenegro, North Macedonia, Romania, Ser- proven vectors of Leishmania spp. in the Old and New bia, Slovenia and Turkey (Eastern Trace). Of these, we World [1]. Leishmaniases, diseases caused by parasitic primarily focused on the former Yugoslavian countries protozoans of the genus Leishmania (Kinetoplastida: and Bulgaria. Trypanosomatidae), infect approximately two million Te present study presents results of entomologi- people annualy, with Latin America, East Africa, Indian cal collections of sand fies in eight countries (Bulgaria, subcontinent, the Middle East and the Mediterranean Bosnia and Herzegovina, Croatia, Kosovo, Montenegro, Basin being among the most afected regions [2]. In North Macedonia, Serbia and Slovenia) through exten- addition to this burden, sand fies also transmit several sive feld studies performed between 2014 and 2016 dur- medicaly important viruses like sand fy fever Sicilian ing the VectorNet Project. We provide the frst checklists and Toscana virus of the genus Phlebovirus and Chand- of sand fy species for several surveyed countries and ipura and Isfaham viruses of the genus Vesiculorivus [1]. updated checklists for the remaining countries. We com- Recent studies in the Mediterranean Basin have shown pare these checklists with the historical records reviewed that the diversity and prevalence of these viruses is much from previously published studies with the aim to criti- higher than previously known [3–5], further highlighting cally assess the past and current species composition of the importance of updated knowledge of sand fy fauna of sand fy fauna in this important yet understudied region. the region. Knowledge of vector species distribution is crucial for Methods the assessment of vector-borne disease risk. Tis was Literature search and data extraction prioritized by European Centre for Disease Prevention Te literature search follows the Prisma Journal Pub- and Control (ECDC) and European Food Safety Author- lishing protocol workfow [6]. PubMed, Web of Science, ity (EFSA), both agencies jointly funding in the periods Ovid Medline, CAB Direct, Google Scholar databases 2010–2014 and 2014–2018, respectively, two consecutive and web searches were screened from 1910 to 2019. Full projects named VborNet and VectorNet. Te enormous text articles, reports, theses, congress presentations, efort to extract presence/absence data from published book chapters in English language containing informa- literature during the VborNet project resulted in a large, tion on phlebotomine sand fies from the Balkan region validated, high-quality dataset of European sand fies. were selected. Other articles, including those published Gap analysis performed to detect possible missing data in other languages that contain valuable information and to determine the areas with less or no information were also included in the data set. Some data on phle- of sand fy species in the Western Palearctic and particu- botomine sand fies also comes from direct consultations larly in Europe revealed several understudied regions with experts and their in-house unpublished databases. including the Balkans. Te apparent lack of updated The following search string was used. Terms in title: information about sand fy fauna, despite records of sand [(phlebotomine OR sandflies OR sand flies) AND in fy-borne diseases in the past as well as recently, is under- all fields: (Phlebotomus OR Sergentomyia) AND in all standable in the light of political and social upheavals in fields: (Phlebotomus OR Paraphlebotomus OR Larrous- this region during the last three decades. Neighboring sius OR Adlerius OR Transphlebotomus) AND in all Mediterranean countries in the west are well known to be fields: (species name) AND in all fields: (distribution endemic for leishmaniasis caused by Leishmania infan- OR presence OR occurrence OR report OR spread OR tum but their sand fy fauna presumably partially difers dispers OR detect) AND in all fields:(“former Yugo- in species composition [1]. Te Balkan region was there- slavia” OR Yugoslavia OR “Balkan region” OR “Medi- fore chosen as a target of a thorough entomological feld terranean area” OR Europe OR Balkans OR “Thrace Dvorak et al. Parasites Vectors (2020) 13:573 Page 3 of 15 Region” OR Trakia OR Trakya OR Bulgaria OR Mac- The study area
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