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      Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe

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          Abstract

          Many factors are involved in determining the latitudinal and altitudinal spread of the important tick vector Ixodes ricinus (Acari: Ixodidae) in Europe, as well as in changes in the distribution within its prior endemic zones. This paper builds on published literature and unpublished expert opinion from the VBORNET network with the aim of reviewing the evidence for these changes in Europe and discusses the many climatic, ecological, landscape and anthropogenic drivers. These can be divided into those directly related to climatic change, contributing to an expansion in the tick’s geographic range at extremes of altitude in central Europe, and at extremes of latitude in Scandinavia; those related to changes in the distribution of tick hosts, particularly roe deer and other cervids; other ecological changes such as habitat connectivity and changes in land management; and finally, anthropogenically induced changes. These factors are strongly interlinked and often not well quantified. Although a change in climate plays an important role in certain geographic regions, for much of Europe it is non-climatic factors that are becoming increasingly important. How we manage habitats on a landscape scale, and the changes in the distribution and abundance of tick hosts are important considerations during our assessment and management of the public health risks associated with ticks and tick-borne disease issues in 21 st century Europe. Better understanding and mapping of the spread of I. ricinus (and changes in its abundance) is, however, essential to assess the risk of the spread of infections transmitted by this vector species. Enhanced tick surveillance with harmonized approaches for comparison of data enabling the follow-up of trends at EU level will improve the messages on risk related to tick-borne diseases to policy makers, other stake holders and to the general public.

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          Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden

          Background Ixodes ricinus is the main vector in Europe of human-pathogenic Lyme borreliosis (LB) spirochaetes, the tick-borne encephalitis virus (TBEV) and other pathogens of humans and domesticated mammals. The results of a previous 1994 questionnaire, directed at people living in Central and North Sweden (Svealand and Norrland) and aiming to gather information about tick exposure for humans and domestic animals, suggested that Ixodes ricinus ticks had become more widespread in Central Sweden and the southern part of North Sweden from the early 1980s to the early 1990s. To investigate whether the expansion of the tick's northern geographical range and the increasing abundance of ticks in Sweden were still occurring, in 2009 we performed a follow-up survey 16 years after the initial study. Methods A questionnaire similar to the one used in the 1994 study was published in Swedish magazines aimed at dog owners, home owners, and hunters. The questionnaire was published together with a popular science article about the tick's biology and role as a pathogen vector in Sweden. The magazines were selected to get information from people familiar with ticks and who spend time in areas where ticks might be present. Results Analyses of data from both surveys revealed that during the near 30-year period from the early 1980s to 2008, I. ricinus has expanded its distribution range northwards. In the early 1990s ticks were found in new areas along the northern coastline of the Baltic Sea, while in the 2009 study, ticks were reported for the first time from many locations in North Sweden. This included locations as far north as 66°N and places in the interior part of North Sweden. During this 16-year period the tick's range in Sweden was estimated to have increased by 9.9%. Most of the range expansion occurred in North Sweden (north of 60°N) where the tick's coverage area doubled from 12.5% in the early 1990s to 26.8% in 2008. Moreover, according to the respondents, the abundance of ticks had increased markedly in LB- and TBE-endemic areas in South (Götaland) and Central Sweden. Conclusions The results suggest that I. ricinus has expanded its range in North Sweden and has become distinctly more abundant in Central and South Sweden during the last three decades. However, in the northern mountain region I. ricinus is still absent. The increased abundance of the tick can be explained by two main factors: First, the high availability of large numbers of important tick maintenance hosts, i.e., cervids, particularly roe deer (Capreolus capreolus) during the last three decades. Second, a warmer climate with milder winters and a prolonged growing season that permits greater survival and proliferation over a larger geographical area of both the tick itself and deer. High reproductive potential of roe deer, high tick infestation rate and the tendency of roe deer to disperse great distances may explain the range expansion of I. ricinus and particularly the appearance of new TBEV foci far away from old TBEV-endemic localities. The geographical presence of LB in Sweden corresponds to the distribution of I. ricinus. Thus, LB is now an emerging disease risk in many parts of North Sweden. Unless countermeasures are undertaken to keep the deer populations, particularly C. capreolus and Dama dama, at the relatively low levels that prevailed before the late 1970s - especially in and around urban areas where human population density is high - by e.g. reduced hunting of red fox (Vulpes vulpes) and lynx (Lynx lynx), the incidences of human LB and TBE are expected to continue to be high or even to increase in Sweden in coming decades.
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            Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus.

            We examined whether a reported northward expansion of the geographic distribution limit of the disease-transmitting tick Ixodes ricinus and an increased tick density between the early 1980s and mid-1990s in Sweden was related to climatic changes. The annual number of days with minimum temperatures above vital bioclimatic thresholds for the tick's life-cycle dynamics were related to tick density in both the early 1980s and the mid-1990s in 20 districts in central and northern Sweden. The winters were markedly milder in all of the study areas in the 1990s as compared to the 1980s. Our results indicate that the reported northern shift in the distribution limit of ticks is related to fewer days during the winter seasons with low minimum temperatures, i.e., below -12 degrees C. At high latitudes, low winter temperatures had the clearest impact on tick distribution. Further south, a combination of mild winters (fewer days with minimum temperatures below -7 degrees C) and extended spring and autumn seasons (more days with minimum temperatures from 5 to 8 degrees C) was related to increases in tick density. We conclude that the relatively mild climate of the 1990s in Sweden is probably one of the primary reasons for the observed increase of density and geographic range of I. ricinus ticks. Images Figure 1 Figure 2 Figure 3
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              An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus.

              The wide geographic and climatic range of the tick Ixodes ricinus, and the consequent marked variation in its seasonal population dynamics, have a direct impact on the transmission dynamics of the many pathogens vectored by this tick species. We use long-term observations on the seasonal abundance and fat contents (a marker of physiological ageing) of ticks, and contemporaneous microclimate at three field sites in the UK, to establish a simple quantitative framework for the phenology (i.e. seasonal cycle of development) of I. ricinus as a foundation for a generic population model. An hour-degree tick inter-stadial development model, driven by soil temperature and including diapause, predicts the recruitment (i.e. emergence from the previous stage) of a single cohort of each stage of ticks each year in the autumn. The timing of predicted emergence coincides exactly with the new appearance of high-fat nymphs and adults in the autumn. Thereafter, fat contents declined steadily until unfed ticks with very low energy reserves disappeared from the questing population within about 1 year from their recruitment. Very few newly emerged ticks were counted on the vegetation in the autumn, but they appeared in increasing numbers through the following spring. Larger ticks became active and subsequently left the questing population before smaller ones. Questing tick population dynamics are determined by seasonal patterns of tick behaviour, host-contact rates and mortality rates, superimposed on a basal phenology that is much less complex than has hitherto been portrayed.
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                Author and article information

                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central
                1756-3305
                2013
                2 January 2013
                : 6
                : 1
                Affiliations
                [1 ]Medical Entomology Group, MRA, Emergency Response Department, Health Protection Agency, Salisbury, UK
                [2 ]Centre for Disease Prevention and Control, Riga, Latvia
                [3 ]Institute of Parasitology, Slovak Academy of Sciences, Kosice, Slovakia
                [4 ]University of Zaragoza, Zaragoza, Spain
                [5 ]Rue de la Voie Sacrée, Souilly, France
                [6 ]Department of Virology, National Institute for Health Development, Tallinn, Estonia
                [7 ]University of Uppsala, Uppsala, Sweden
                [8 ] , Nolsoy, Faroe Islands
                [9 ]University of Copenhagen, Copenhagen, Denmark
                [10 ]Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia
                [11 ]Hospital San Pedro - Centro de Investigación Biomédica de La Rioja, Logroño, Spain
                [12 ]Aristotle University of Thessaloniki, Thessaloniki, Greece
                [13 ]Ludwig-Maximilians-University Munich, Munich, Germany
                [14 ]Institut National de la Recherche Agronomique, Ecole Nationale Vétérinaire, Agroalimentaire et de l'Alimentation, Nantes, France
                [15 ]University of Oxford, Oxford, UK
                [16 ]Fondazione Edmund Mach, San Michele all’Adige, TN, Italy
                [17 ]Instituto Nacional de Saúde Dr. Ricardo Jorge, CEVDI, Lisboa, Portugal
                [18 ]National Institute of Public Health and Environment (RIVM), Bilthoven, Netherlands
                [19 ]CIRAD, Montpellier, France
                [20 ]Avia-GIS, Zoersel, Belgium
                [21 ]European Centre for Disease Prevention and Control, Stockholm, Sweden
                Article
                1756-3305-6-1
                10.1186/1756-3305-6-1
                3549795
                23281838
                a1dbac5c-fa93-4c57-942d-30555eccfb1c
                Copyright ©2013 Medlock et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 November 2012
                : 10 December 2012
                Categories
                Review

                Parasitology
                tick,ixodes,europe,distribution,climate,ecology,surveillance,tick-borne disease
                Parasitology
                tick, ixodes, europe, distribution, climate, ecology, surveillance, tick-borne disease

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