07_Akimov_05_2022.indd UDC 595.421(477) DISTRIBUTION OF IXODES RICINUS (ARACHNIDA, IXODIDAE) IN UKRAINE IN THE CONTEXT OF TICK HAZARD, AND FACTORS FAVORING ITS PERSISTENCE IN CONDITIONS OF FAST-GOING ENVIRONMENTAL CHANGE I. A. Akimov†1, I. V. Nebogatkin†1,2 1Schmalhausen Institute of Zoology NAS of Ukraine, vul. B. Khmelnytskogo, 15, Kyiv, 01030 Ukraine 2SI Public Health Center of the MoH of Ukraine vul. Yaroslavska, 41, Kyiv, 04071 Ukraine E-mail: zoodiversity@izan.kiev.ua I. A. Akimov (https://orcid.org/ 0000-0001-9025-2612) I. V. Nebogatkin (https://orcid.org/0000-0003-1451-462X) Distribution of Ixodes ricinus (Arachnida, Ixodidae) in Ukraine in the Context of Tick Hazard, and Factors Favoring its Persistence in Conditions of Fast-Going Environmental Change. Akimov, I. A., Nebogatkin, I. V. — Habitat conditions and factors were studied contributing to the spread of Ixodes ricinus (Linnaeus, 1758) over vast territories. Th ere are excellent conditions for the existence of the hard ticks in the settlement agglomerations throughout Ukraine: suitable biotopes with expedient litter and a large number of hosts for all stages of development of ticks. Th e castor bean tick lives in all of Ukraine, adapting its size of idiosome and diapause to changing environmental conditions, and using the ability to parasitize on animals well adapted to urban conditions. Ixodes ricinus prefers urban landscapes in areas with unfavorable environmental conditions. Th e hiatus in the range of the castor bean tick between the southern mainland of Ukraine and the steppe regions of Crimea may be restored due to global climatic changes. K e y w o r d s : ticks, Ixodes ricinus, distribution, urban landscapes, Ukraine. Introduction Th e castor bean tick Ixodes ricinus (Linnaeus, 1758) is the most abundant species of hard ticks in Europe. Th e southern border of its range is along the borders of Turkey and several northern African countries. Th e eastern border is in the Russian Federation (Lindquist & Vapalahti, 2008), and the northern one is expanding northward due to climate warming (Medlock et al., 2013). Th e hiatus (fi g. 1) in the range that has been noted on the territory of Ukraine (Akimov & Nebogatkin, 1996) disappeared in 1980–1990s (Akimov & Nebogatkin, 1996). Th e species now lives throughout the country except for typically arid landscapes (Akimov & Nebogatkin, 2010). As the only common species of the subgenus Ixodes, I. ricinus is the vector of spirochetes of the genus Borrelia (complexes of B. burgdorferi s. l. and B. miyamotoi s. l.) in Ukraine (Filippova, 1990; Rogovskiy et al., 2018). Hence, it transmits the most common illness in humans and domestic animals, associated with ixodids, Lyme disease (Korenberg et al., 2016; Nebogatkin & Shulhan, 2020). Th e aims of the present work are to present the distribution of I. ricinus in Ukraine in view of tick hazard starting from the beginning of XXI century, to fi nd out the reasons for the “prosperity” of the species under conditions of fast-going environmental change, and to assess the current state of the former hiatus at the territory in Ukraine. Zoodiversity, 56(5):429–434, 2022 DOI 10.15407/zoo2022.05.429 430 I. A. Akimov, I. V. Nebogatkin Fig.1. Th e hiatus in the range that has been noted on the territory of Ukraine : 1 — European area of distribution; 2 — Crimean area of distribution; 3 — Caucasian-Western Asian area of distribution; 4 — zone of disjunction (aft er fi g. 1 Akimov & Nebogatkin, 1996 with changes). T a b l e 1 . Data used to compile a tick hazard map for humans and animals on the example of I. ricinus No Plots Quantity regions Quantity district I. ricinus feeders ID I. ricinus fl ag ID AI 1 Eastern Polissia 2 21 83 858 28.53 8636 20.28 3 2 Central Polissia 2 23 28 747 71.15 8402 46.99 5 3 Western Polissia 4 29 44 227 54.59 29 713 28.51 4 4 Eastern Forest-steppe 4 54 67 80 25.71 34 949 46.66 4 5 Central Forest-steppe 4 90 37 107 58.79 40140 58.74 5 6 Western Forest-steppe 7 55 60 360 82.28 49 696 50.91 5 7 Northwestern F-S 2 13 31 860 67.30 23 031 38.94 4 8 Eastern Steppe 4 42 6576 21.98 3696 48.63 3 9 Left Bank Steppe 4 42 9260 62.07 13 778 47.12 4 10 Donets Ridge 2 12 4209 20.58 960 12.32 2 11 Right Bank Steppe 5 66 172 324 62.07 18 424 51.46 5 12 Seaside Steppe 1 2 569 6.77 724 11.93 1 13 Carpathians Mountains 4 16 10 758 70.63 4238 66.10 5 14 Carpathians Foothills 4 14 27 178 60.7 3660 85.16 5 15 Crimea Foothills 1 4 127 2.62 58 30.95 2 16 Crimea Steppe 1 10 36 0.23 56 9.16 1 17 Crimea Kerch 1 1 4 0.17 16 2.59 1 18 Crimea Mountains 1 3 324 11.53 602 53.98 5 Total 53 497 52 4304 37.35 240 779 37.50 64 N o t e . ID — index of dominance; AI — average indicator. Material and methods Th e studies were carried out using a fl ag or combing from small mammals, or by manual collection from the domestic and agricultural animals according to standard methods (Tularemia, 1954). We used our own data and materials from six-month forecasts and reviews of the Public Health Center of the Ministry of Health of Ukraine, which has previously been known also as Ukrainian Center for Disease Control and Monitoring, Ukrainian Center for State Sanitary and Epidemiological Surveillance, and Republican Sanitary and Epidemiological Station of the Ministry of Health of the Ukrainian SSR. Th e territory of Ukraine has been divided into 18 landscape-geographical areas (table 1) according to the boundaries of the administrative regions as of July 17, 2020 (Akimov & Nebogatkin, 2011). Th e total number of ticks was summed up for the period of 2000–2020 to calculate the index of dominance, ID (Beklemishev, 431Distribution of Ixodes ricinus (Arachnida, Ixodidae) in Ukraine in the Context of Tick Hazard… 1961). Based on the index value, tick abundance was scored from 1 to 5 at each landscape-geographical area for the collection from animals and for counts on the fl ag separately. Aft er that, the results were summarized and averaged. In order to understand the fl ourishing of the species under the conditions of the fast environmental changes, we grouped the studied territories of dacha cooperatives, widespread in suburbs of large cities and towns of Ukraine, into settlement agglomerations. We used own data obtained during 16 years starting from 2005 at 3 sites of Kyiv Region, including natural biotopes, part of settlement agglomerations of Kyiv City and Bila Tserkva town. Th e maps were made in QGIS 3.16. Th e statistical processing was performed in the programs R-statistics i386 3.5.1 and Past 3.2. Results and discussion We analyzed the distribution of 524 304 I. ricinus ticks collected from hosts, and 240 779 ticks caught on the fl ag. In total, 765 083 pieces were analyzed according to the summarized data taken from six-month forecasts and our own data since 2000 (table 1). Th e percentage of ticks collected by authors to the total number varied depending on the site from 0.3 % (Carpathian Mountains) to 45 % (central Forest-steppe and Polissia). Th ree sites were found with a very low abundance (1 point), two sites with a low (2 points) and with an average abundance (3 points), 4 sites with normal abundance (4 points) and 7 sites (5 points) with a lot of castor bean ticks. Th e optimum (4 and 5 points) of the abundance of I. ricinus in Ukraine was found on the territory of 11 areas of 20 regions (fi g. 2), or 61.11 %. Th us, the distribution of the castor bean tick at the territory of Ukraine diff ers in terms of abundance, the level of dominance, and the presence of foci of mass tick emergence, i. e. in terms of tick hazard. Th e territory of Ukraine is divided into four following zones according to the distribution of I. ricinus: • zone of dominance of the castor bean tick by abundance factor over other ixodid species, ID more than 50 %; Fig. 2. Distribution of I. ricinus on the territory of Ukraine, from the point of view of tick-borne danger. 432 I. A. Akimov, I. V. Nebogatkin • zone of regularly occurring mass emergence, once in three years; • zone of periodically occurring mass emergence; • zone of mosaic foci of emergence due to unfavorable environmental conditions. To study the ecology of ixodid ticks in the settlement agglomerations, more than 300 fi eld trips were carried out, about 20 thousand ixodid ticks of 3 species were captured, 345 Gero traps were placed, and 67 small mammals of 4 species were caught in Kyiv Region (table 2). A paired two-sample t-test for averages in pairwise comparison of the results for areas with a normal distribution showed a signifi cant diff erence by more than 95 % between natural biotopes, Kyiv and Bila Tserkva agglomerations. Th e abundance of I. ricinus in the Bila Tserkva agglomeration is more than twice higher (P > 0.05) than that in natural biotopes, and more than in the Kyiv agglomeration. Th e fi nds of I. hexagonus Leach, 1815 indicate the existence of Southern white-breasted hedgehogs (Erinaceus concolor Martin, 1838) in these territories, and their abundance is apparently higher in the human-altered landscapes. Among small mammals in settlement agglomerations Apodemus agrarius (Pallas, 1771) are dominant, amounting to 6.67 per 100 п/с (ID is 62.16) and house mice (Mus musculus Linnaeus, 1758), amounting to 2.32 п/с (ID is 21.62). Single specimen’s genus of Sylvaemus Ognev, and common shrews (Sorex araneus Linnaeus, 1758) were recorded in the catches: 0.87 per 100 trap-days. One of the three wood mouse (Sylvaemus sylvaticus (Linnaeus, 1758)) was a host of one non- feeding and two feeding nymphs of I. ricinus. Th us, there are excellent conditions for the existence of ixodid ticks at the settlement agglomerations of Ukraine, there are suitable biotopes with expedient litter, varying grasses and thickets of ruderal plant species, a lot of hosts of all stages of tick development, including stray and domestic dogs and cats, large and small ruminants, horses, various species of mice and shrew hosts of immature ticks. In Ukraine, the number of castor bean ticks is higher in urban landscapes than in natural ones, even higher than in settlement agglomerations. One of the reasons for this fact can be elimination of roe deer in many habitats except for hunting grounds. Th us, the most important factors that determine the prosperity of I. ricinus in most of its range are, in our opinion: 1. Th e size of the idiosomes of mature and immature ticks are 3–4 mm. Th at allows inhabiting the biotopes with relatively low humidity (up to 75 %) due to the ability of litter to adsorb water vapor above the soil surface. To accumulate water, the mature I. ricinus ticks enter the litter on soil surface, from 1 to 8 times, depending on microclimate (Gigon, 1985). Th e tick salivary glands produce hyperosmotic saliva in alveoli of the 1st order (Needham et al., 1990). Th is saliva actively collects water vapor from the air. Th e vapor is adsorbed in the preoral cavity. Droplets of the hygroscopic saliva are then swallowed back or adsorbed in certain cuticle areas inside the oral cavity (Rudolph, Knulle, 1978). Also, ticks can exist in small islands of natural and artifi cial landscapes, including urban, scattered mosaically, on a wide range of hosts of various sizes. 2. Using diapause, the castor bean tick can complete its full life cycle in 1.5 to 5–10 years, allowing for signifi cant individual longevity (Balashov, 1998). During this time, they avoid elimination by possible acaricidal treatments or several consequent dry years in a row, T a b l e 2 . Abundance indices of ixodid ticks and the sampling eff ort in three areas of Kyiv Region Plots Sections Number of ticks Species IR DR IH Vasilkovsky District, natural biotopes 77 8298 4,44 5,03 not diff er Kyiv-Sviatoshyn agglomeration 125 9554 6,60 5,10 0,01 Bilotserkivsky agglomeration 59 8895 10,38 11,73 0,03 N o t e . IR — I. ricinus; DR — D. reticulates; IH — I. hexagonus. 433Distribution of Ixodes ricinus (Arachnida, Ixodidae) in Ukraine in the Context of Tick Hazard… and survive in conditions of newly developed areas and otherwise changing environment (Akimov & Nebogatkin, 2016). 3. Th e ability of ticks at all stages of development to parasitize on animals that are most adapted to urban and anthropogenic landscapes. Th ese hosts include the fi eld and house mice, the brown rat (small mammals); foxes (carnivores); cats and dogs, including stray; domestic and agricultural cattle (goats, cows, horses). 4. Parasitizing birds, including common passerines, provides access to new territories. Adults of Parus major Linnaeus, 1758 and, more oft en, the younger birds of this species fl y hundreds of kilometers away for wintering. Th ose birds migrate mainly from west to east than from north to south and back (Poluda, 2011). In such areas, ixodid ticks can create spontaneous foci (Nebogatkin, 1996), which either become permanent or decline. 5. Ticks inhabit the relatively new conditions of settlement agglomerations, which are spreading, including on the territories which ixodid ticks did not previously live due to low moisture. Natural warming of the planet’s climate, on the one hand, ensures that several species of ixodid ticks expand northward, such as Ixodes persulcatus Schulze, 1930 (Uspensky et al., 2003), and Ixodes ricinus (Medlock et al., 2013). On the other hand, the warming induces unfavorable conditions associated with the loss of moisture in habitats in parts of the species ranges located closer to the equator. Hence, a natural interest arose in the areas of the former hiatus of this species on the territory of Ukraine (Nebogatkin, 2018). Findings the castor tick in the southern regions of Ukraine confi rm the existence of local foci of reproduction of the species. Th e index of dominance ranged from 0.06 to 14.7 (table 1). Th e presence of this species is indirectly confi rmed by human cases of Lyme disease (Rogovskiy et al., 2020). In 2009–2019, the number of cases of Lyme disease in Kherson region was 12 times less than in Kyiv Region. In the southern regions of Ukraine, I. ricinus is inhabiting local areas, urban territories, and settlement agglomerations near large and medium-sized cities. However, due to climate change, conditions for the hiatus in the range of I. ricinus in Ukraine may reappear. Conclusions Th e castor bean tick (Ixodes ricinus) lives everywhere in Ukraine, adapting to changing environmental conditions based on the size of its idiosome, diapause, the ability to parasitize on mammals and birds well adapted to urban conditions, especially in settlement agglomerations. In areas with unfavorable environmental conditions, I. ricinus tends to inhabit urban landscapes. Continuous ranges of ixodid ticks should be modeled as separate zones based on the level of tick hazard, taking into account dominance, the possibility of regular, periodic mass foci of reproduction, and mosaic habitats. References Akimov, I., Nebogatkin, I. 2011. Distribution of ticks from of the genus Dermacentor (Acari, Ixodidae) in Ukraine. Vestnik Zoologii, 45 (1), 35–40. DOI: DOI 10.2478/v10058-011-0001-x. Akimov, I. A., Nebogatkin, I. V. 1996. On the southern border of distribution of the sheep tick (Ixodes ricinus L.). Vestnik Zoologii, 6, 84–86. Akimov, I. A., Nebogatkin, I. V. 2010. Seasonal Changes in Activity, Sex Composition and Areal of the Tick Ixodes ricinus (Acari, Ixodida) in the Landscape-Geographical Regions of Ukraine. Vestnik Zoologii, 44 (3), 245–251. DOI: DOI 10.2478/v10058-010-0014-x. Akimov, I. А., Nebogatkin, I. V. 2016. Ixodid Ticks (Acari, Ixodidae) in Urban Landscapes. A review. Vestnik Zoologii, 50 (2), 155–162. DOI: 10.1515/vzoo-2016-0018. Balashov, Y. 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Received 9 February 2021 Accepted 28 October 2022 << /ASCII85EncodePages false /AllowTransparency false /AutoPositionEPSFiles true /AutoRotatePages /None /Binding /Left /CalGrayProfile (Dot Gain 20%) /CalRGBProfile (sRGB IEC61966-2.1) /CalCMYKProfile (U.S. Web Coated \050SWOP\051 v2) /sRGBProfile (sRGB IEC61966-2.1) /CannotEmbedFontPolicy /Error /CompatibilityLevel 1.4 /CompressObjects /Tags /CompressPages true /ConvertImagesToIndexed true /PassThroughJPEGImages true /CreateJobTicket false /DefaultRenderingIntent /Default /DetectBlends true /DetectCurves 0.0000 /ColorConversionStrategy /CMYK /DoThumbnails false /EmbedAllFonts true /EmbedOpenType false /ParseICCProfilesInComments true /EmbedJobOptions true /DSCReportingLevel 0 /EmitDSCWarnings false /EndPage -1 /ImageMemory 1048576 /LockDistillerParams false /MaxSubsetPct 100 /Optimize true /OPM 1 /ParseDSCComments true /ParseDSCCommentsForDocInfo true /PreserveCopyPage true /PreserveDICMYKValues true /PreserveEPSInfo true /PreserveFlatness true /PreserveHalftoneInfo false /PreserveOPIComments true /PreserveOverprintSettings true /StartPage 1 /SubsetFonts true /TransferFunctionInfo /Apply /UCRandBGInfo /Preserve /UsePrologue false /ColorSettingsFile () /AlwaysEmbed [ true ] /NeverEmbed [ true ] /AntiAliasColorImages false /CropColorImages true /ColorImageMinResolution 300 /ColorImageMinResolutionPolicy /OK /DownsampleColorImages true /ColorImageDownsampleType /Bicubic /ColorImageResolution 300 /ColorImageDepth -1 /ColorImageMinDownsampleDepth 1 /ColorImageDownsampleThreshold 1.50000 /EncodeColorImages true /ColorImageFilter /DCTEncode /AutoFilterColorImages true /ColorImageAutoFilterStrategy /JPEG /ColorACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /ColorImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000ColorACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000ColorImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasGrayImages false /CropGrayImages true /GrayImageMinResolution 300 /GrayImageMinResolutionPolicy /OK /DownsampleGrayImages true /GrayImageDownsampleType /Bicubic /GrayImageResolution 300 /GrayImageDepth -1 /GrayImageMinDownsampleDepth 2 /GrayImageDownsampleThreshold 1.50000 /EncodeGrayImages true /GrayImageFilter /DCTEncode /AutoFilterGrayImages true /GrayImageAutoFilterStrategy /JPEG /GrayACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /GrayImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000GrayACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000GrayImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasMonoImages false /CropMonoImages true /MonoImageMinResolution 1200 /MonoImageMinResolutionPolicy /OK /DownsampleMonoImages true /MonoImageDownsampleType /Bicubic /MonoImageResolution 1200 /MonoImageDepth -1 /MonoImageDownsampleThreshold 1.50000 /EncodeMonoImages true /MonoImageFilter /CCITTFaxEncode /MonoImageDict << /K -1 >> /AllowPSXObjects false /CheckCompliance [ /None ] /PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false /PDFXNoTrimBoxError true /PDFXTrimBoxToMediaBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXSetBleedBoxToMediaBox true /PDFXBleedBoxToTrimBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXOutputIntentProfile () /PDFXOutputConditionIdentifier () /PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False /CreateJDFFile false /Description << /ARA /BGR /CHS /CHT /CZE /DAN /DEU /ESP /ETI /FRA /GRE /HEB /HRV (Za stvaranje Adobe PDF dokumenata najpogodnijih za visokokvalitetni ispis prije tiskanja koristite ove postavke. 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