Judging by the results of blood-PCR, the recipient mice developed bacteremia within seven days after placement of Bartonella-infected ticks and remained bacteremic at least until day 16. This work represents the first in vivo demonstration of a Bartonella sp. https://doi.org/10.1371/journal.pone.0189092.s004, https://doi.org/10.1371/journal.pone.0189092.s005, https://doi.org/10.1371/journal.pone.0189092.s006. Citation: Alkishe AA, Peterson AT, Samy AM (2017) Climate change influences on the potential geographic distribution of the disease vector tick Ixodes ricinus. Here, we assessed the potential distribution of I. ricinus under current and future climate conditions to understand how climate change will influence the geographic distribution of this important tick vector in coming decades. Yes Previous studies of the potential distribution of I. ricinus have generally covered small geographic areas [15, 16], such as some studies in single countries that have attempted to understand the population dynamics of this species [17, 18]. gibosus, Dermacentor species and Haemaphysalis species have also been implicated. Funding: AAA was supported by the Ministry of Higher Education, Libya. We chose Spain as a reasonable intermediate-density reference point (6 occurrence records /100,000 km2) to overcome problems associated with oversampling or undersampling observed in some countries. or Babesia spp., suggesting that these might be co-transmitted by the same vectors –. The final balanced dataset of I. ricinus included 416 occurrence points, which we separated five times randomly into equal-sized subsets of 208 points, one subset was for model calibration and the other for model evaluation (Fig 1). École Nationale Vétérinaire d'Alfort, Centre de Recherche Biomedicale, Maisons-Alfort, France, Affiliation here. PLoS Negl Trop Dis 5(5): Increased TBE transmission in Europe during the last 2 decades has been attributed to climate change, socio-economic changes, and anthropogenic activities . Writing – review & editing, Affiliation Nymphs fed as larvae upon the B. birtlesii-infected mouse were placed on naïve uninfected mice at approximately 3 months after the molt in order to evaluate bacterial transmission from ticks to mice. Humans can be infected with Lyme disease (caused by Borrelia burgdorferi), Q fever (caused by Coxiella burnetti), the viral infection 'louping ill' and (most dangerously) tick-borne encephalitis. B. birtlesii DNA was detected in samples drawn on days three through eight of tick attachment (Figure 2), indicating that adult ticks were successfully emitting the bacteria into the previously uninfected blood during feeding. Of these, a total of 11 ticks fed to repletion – three, two and six from each of the mice. The medically most important of these pathogens are the TBE virus (TBEV) causing tick-borne encephalitis (TBE) and the Borrelia burgdorferi sensu lato (s.l.) Yes It is a three-host tick. Vector Borne Zoonotic Dis 2010; 10:723–730. Under RCP 4.5, MOP detected extrapolative conditions in as many as 10 of 17 models in both 2050 and 2070. Fig. https://doi.org/10.1371/journal.pntd.0001186.g003. here. Bartonella birtlesii (IBS325T strain ) was grown on 5% defibrinated sheep blood Columbia agar plates (CBA) incubated at 35°C with 5% CO2. transmission by ticks. (2) The data were further filtered by distance, so that all redundant records occurring in a single 10’ cell (~20 km) were omitted. land use, soil characteristics), and biotic factors (e.g., host abundance and competition with other species), should be considered in tandem with climate effects [40–44]. are facultative intracellular vector-borne bacteria associated with several emerging diseases in humans and animals all over the world. Writing – original draft, Validation, During the past 3–4 decades, average temperature has increased, supporting more favourable conditions for ticks. https://doi.org/10.1371/journal.pntd.0001186.g002. This concentration is the one that could be encountered in an infected cats, however, the experimental model remains an experimental model and does not reproduce ideally the natural conditions of pathogen transmission using ticks and animals and therefore, the vector competence of ticks could not be definitively established. Also, we used diverse data sources, and focused on Europe, North Africa, and the Middle East, to develop predictions of the potential distribution of this tick species into the future. Yes No, Is the Subject Area "Ticks" applicable to this article? Formal analysis, The present study used live hosts as both the source and the recipients of bacterial infection in order to confirm vector competence of I. ricinus for a Bartonella sp. No, PLOS is a nonprofit 501(c)(3) corporation, #C2354500, based in San Francisco, California, US, https://doi.org/10.1371/journal.pntd.0001186. Ixodes ricinus, the castor bean tick, is a chiefly European species of hard-bodied tick. The B. birtlesii strain used in this study was a low passage isolates from a field mouse Apodemus sp. PCR detected the presence of Bartonella spp. These results confirm the vector competence of I. ricinus for B. birtlesii and represent the first in vivo demonstration of a Bartonella sp. Conceptualization, We used the data layers at 10’ spatial resolution because of the continental extent of our models. black dots) but none coincided with the 416 records used in model calibration (i.e. ricinus adult females lay large numbers of eggs that hatch into larvae. ovatus, Ix. are facultative intracellular gram-negative bacteria, which commonly infect mammals, particularly rodents. We obtained data on 19 “bioclimatic” variables from the WorldClim climate data version 1.4  available via www.worldclim.org. Detection of Bartonella in 6-day old liquid medium cultures inoculated with blood of a mouse fed upon by B. birtlesii-infected I. ricinus nymphs by A. semi-nested PCR. Third, newly suitable areas must be accessible to I. ricinus via dispersal for actual range expansions to take place . For more information about PLOS Subject Areas, click https://doi.org/10.1371/journal.pone.0189092, Editor: R. Mark Wooten, University of Toledo College of Medicine and Life Sciences, UNITED STATES, Received: June 2, 2017; Accepted: November 18, 2017; Published: December 5, 2017. After 5 days, bacteria were harvested and suspended in sterile phosphate-buffered saline (PBS) immediately before being used for mouse infection. Transferring models to future conditions, the present-day and future distributional patterns largely coincided. Medical Entomology Laboratory, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America. 5 combinations based on the 5 subsets of occurrence records), which summarizes uncertainty deriving from the particular availability of occurrence data. We used Maxent’s bootstrap function to create 10 replicate analyses. Is the Subject Area "Ricinus" applicable to this article? transmission by ticks. AMS was supported by the Graduate Fulbright Egyptian Mission Program (EFMP). No, PLOS is a nonprofit 501(c)(3) corporation, #C2354500, based in San Francisco, California, US, https://doi.org/10.1371/journal.pone.0189092, https://doi.org/10.6084/m9.figshare.5067373, http://ecdc.europa.eu/en/healthtopics/vector/vector-maps/, http://shiny.conabio.gob.mx:3838/nichetoolb2/. B. birtlesii was also detected in the same samples by immunofluorescence (Figure 1B). SGs were collected from different tick life stages fed on various animal species, including cofeeding of nymphs and adults on the same host. Numerous data have been published to date regarding identification of Bartonella DNA in both engorged ticks collected from their natural hosts and questing ticks collected from the environment (for detailed reviews see , ). Specific immune serum was generated by subcutaneous injection immunization of a Balb/C mouse (Charles River Laboratories, L'Arbresle, France) with 108 CFU of B. birtlesii after a freeze-thaw step, and with a boost two weeks later. Under RCP 8.5 for the 2050, the expansions in Eastern and Northern Europe, Turkey, and the Middle East were predicted to be wider compared to RCP 4.5 for 2050. However, a national density map of I. ricinus is still missing. by ticks to a susceptible animal was reported in 1926 by Noguchi who described experimental transmission of B. bacilliformis by Dermacentor andersoni . We first used the jackknifing function in Maxent to identify the most important set of environmental variables. Climate change may affect the seasonal activities and feeding behavior of the different life stages of I. ricinus [34, 35]. Sampling was concentrated in Great Britain and Germany thanks to surveillance by the European Vector Map Program of the European Center for Disease Prevention and Control (ECDC; http://ecdc.europa.eu/en/healthtopics/vector/vector-maps/). Background: Ixodes ricinus is a species of hard tick that transmits several important diseases in Europe and North Africa, including Lyme borreliosis and tick-borne encephalitis. Therefore, the prevalence of infection in molted ticks and the efficiency of transstadial transmission could not be accessed directly. https://doi.org/10.1371/journal.pone.0189092.s003. Both species have a wide spectrum of hosts. Under RCP 8.5, MOP detected extrapolative conditions in 11 and 13 of 17 models in 2050 and 2070, respectively. The work is made available under the Creative Commons CC0 public domain dedication. Therefore, a delay in detection of Bartonella in the blood used for tick feeding may be due to (a) a necessary reactivation period, (b) a 48-hour delay in initiation of actual tick feeding, or (c) a gradual increase of the number of attached feeding ticks and consequently of the volume of infected tick saliva injected into the feeder. For instance, rising temperatures could lead to milder winter conditions, extending spring and fall seasons in northern regions, making them more suitable for I. ricinus. On the other hand, all four of the partially engorged female ticks examined at 72 hours after placement on a membrane feeder contained bacteria in the muscle and salivary gland tissues, but not in the midgut. Half of the liver was stored at −80°C, the other part was homogenized in 500 µL of F12 medium (Invitrogen, Cergy Pontoise, France). Once Bartonella spp DNA had been detected in blood, four females were removed and used for immunohistological assay. The lack of B. birtlesii in the midgut of feeding ticks and its presence in the salivary glands confirms that its transmission to the host occurs with saliva and not through contaminated feces. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. In addition, a number of studies have reported co-infections in both humans and animals with Bartonella spp. For RCP 8.5 for the 2050s, high uncertainty was restricted to southern Finland, eastern Sweden, southern Spain, and northern Morocco; low uncertainty areas were in Western Europe and the Middle East. No, Is the Subject Area "Ixodes" applicable to this article? Yes For further evaluation of our predictions regarding the occurrence of I. ricinus, we used a set of 3186 I. ricinus records discarded during the early phases of data filtering of the original dataset. Blood samples were collected from the retro orbital sinus at seven, thirteen and nineteen days post infection, and the presence of Bartonella DNA was confirmed by semi-nested PCR as previously described . Many tick-borne diseases (TBDs) are so-called meta-zoonoses, i.e., they may be transmitted to humans as well as animals via their invertebrate tick host ().In temperate/cold regions of Europe, the hard tick Ixodes ricinus is the most important vector of TBDs in terms of both animal and human (public) health, followed by Dermacentor reticulatus and Dermacentor marginatus (). may possibly be transmitted by ticks has been debated for several years. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Iceland is located in the North Atlantic Ocean with subpolar oceanic climate. This thresholding approach omitted the 5% of records with the lowest suitability to account for the reality that such large datasets often include some errors (either in the occurrence data or the environmental data), so this 5% trimming allows those errors to be ignored and not affect the results. Yes To date, few studies have investigated effects of climate change on the spatial distribution of I. ricinus at continental extents. This warming is expected to influence vectors and reservoir hosts, in turn affecting the epidemiology of the vector-borne pathogens [11, 12]. Second, other abiotic factors (e.g. The testing records are those retained from the original occurrences (i.e. Ecological niche models (ENMs) were estimated based on the maximum entropy algorithm implemented in Maxent 3.3.3k . 2, 3) and bacteria (e.g., Anaplasma, Rickettsia and Borrelia spp. No, Is the Subject Area "Larvae" applicable to this article? Nymphs, infected at the larval stage, were able to inject B. birtlesii into mice, which in turn became bacteremic. Roles https://doi.org/10.1371/journal.pone.0189092.g001. Ixodes ricinus and Ixodes persulcatus The Ixodes ricinus tick is the most common tick in Northern Europe and is held responsible for Lyme disease transmission to both livestock and humans. here. For present-day conditions, an uncertainty index was derived from the range (maximum—minimum) of predictions from 5 Maxent runs (i.e. Results of the study confirm the vector competence of I. ricinus and represent the first in vivo demonstration of a Bartonella sp. In Sweden, for example, the climate has changed to be significantly warmer in the last 3 decades: the 8 warmest Novembers on record were between 2000 and 2009 . and one of the main vectors of tick-borne encephalitis (TBE) virus. Given that LB, TBE, and various other tick-borne diseases cause serious health problems, predicting future suitable areas for I. ricinus can help to guide plans to manage and mitigate effects of these public health threats . Active surveillance of both diseases in Europe indicates a need to study the distributional ecology of their vector, I. ricinus. When we placed a cohort of infected adult ticks on a membrane feeder, Bartonella DNA was detected in all samples of the used blood removed later than 72 hours, but not in those tested at 24 and 48 hours. PLOS ONE promises fair, rigorous peer review, We did not include western Asia in our study owing to a lack of sufficient occurrence data from this region. To summarize the model results for present-day conditions, we calculated the median of the medians from the predictions based on the 5 subsets of occurrences as an estimate of the current geographic distribution of I. ricinus. Thus, whereas the results of the two studies did not differ qualitatively, our work provides a clearer picture of certainty and uncertainty in these predictions for an important disease vector species. Detection of B. birtlesii in adult I. ricinus salivary glands (A, B) and muscle tissues (C, D) sections colored with hemalun-eosin, by histochemical staining: A & C – uninfected ticks; B & D – infected ticks. A Dermacentor sp. We obtained parallel data layers for 17 general circulation models (GCMs; Table 1) for each representative concentration pathway (RCP) for each time period. PCR amplification of Bartonella spp. No, Is the Subject Area "Blood" applicable to this article? Lines D0, D7, and D16 represent blood samples taken on days 0, 7, and 16 after tick placement respectively; T+ – B. birtlesii DNA; M – molecular mass marker. values outside of the range of environments in the reference region/time) occurs, to give a view of certainty and uncertainty across various sectors of the region of interest . Climate change is affecting the geographic distributions and abundances of arthropod vectors, which in turn influence the geographic distribution and epidemiology of associated vector-borne diseases. For more information about PLOS Subject Areas, click First, as with all ixodid ticks, I. ricinus spends most of its life cycle off the host and in the environment, so climate change may have direct effects on its abundance and distribution . Left-hand panels show the average MOP distance among models (dark red represents high average and dark blue represents low average). Institut National de la Recherche Agronomique, USC INRA Bartonella-Tiques, ANSES, Maisons-Alfort, France, Affiliation Histochemical staining showed the presence of bacteria in salivary glands and muscle tissues of partially engorged adult ticks, which had molted from the infected nymphs. Ixodes ricinus is an important disease vector in Europe. Calibrating models for I. ricinus based on the 5 subgroups of occurrence points yielded predictions that gave area under the curve (AUC) ratios above null expectations in all five partial ROC analyses (P < 0.001; S2 File). Larval and nymphal I. ricinus were fed on a B. birtlesii-infected mouse. Any extrapolative transfer of the model should be interpreted with considerable caution. As various Bartonella spp are common in wild and domestic animals, acquisition of these erythrocyte associated microorganisms by feeding ticks with a blood meal can be expected, and thus detection of bacterial DNA in engorged or partially engorged ticks does not add to the debate. Indeed, although it is believed that most Bartonella spp. For future conditions, we calculated medians across all single-GCM median model outputs (5 subsets of occurrences x 17 GCMs = 85 combinations), as an estimate of the potential distribution of I. ricinus under each corresponding RCP. There has been considerable research carried out over nearly a hundred years on […] No, Is the Subject Area "Ecological niches" applicable to this article? Entomology Department, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt. We used diverse GCMs available from the WorldClim archive to estimate both the future distributional potential of I. ricinus based on each individual GCM, which was a key element in assessing uncertainty in predictions deriving from GCM choice. https://doi.org/10.1371/journal.pone.0189092.t001. 250 µL of the homogenate were spread on CBA plates incubated at 35°C with 5% CO2. In addition, we included mobility-oriented parity (MOP) to understand certainty and uncertainty in different areas in the region of interest . Four cDNA samples were sequenced, We determined whether Ixodes ricinus, the major vector for Lyme borreliosis in Western Europe, also express salp15-related genes. Yes Ixodes ricinus, primarily associated with deciduous and mixed forests, is the principal vector of causative agents of viral, bacterial and protozoan zoonotic diseases in Europe. Ixodes scapularis is the main vector of Lyme disease in North America. The larvae and nymphs parasitize many different animal species, including large animals such as deer, but tend to make most contact with hosts that move within the vegetation cover. Ix. https://doi.org/10.1371/journal.pntd.0001186, Editor: David H. Walker, University of Texas Medical Branch, United States of America, Received: December 12, 2010; Accepted: April 14, 2011; Published: May 31, 2011. with large numbers of the key vector species underlies this importance. Identical results were obtained for all three recipient mice in both assays. https://doi.org/10.1371/journal.pone.0189092.g003. The molting success of larvae fed upon a Bartonella-infected mouse was low, and molted nymphs were not tested due to their paucity. Birtlesii -infected mouse ; refs from diverse sources 3–4 decades, average has. Taken on days 0, 7, and eastern Belarus collection and ixodes ricinus vector, decision to publish or. 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Can also transmit other Borrelia species, including Borrelia miyamotoi made similar future projections for I. ricinus at extents. The uncertainty efforts were made to minimize suffering of animals oceanic climate to nymphal and stage... 5, 6 ] ticks to survive the winter, and molted nymphs were not tested to... Derived from the range ( maximum—minimum ) of predictions from 5 Maxent runs ( i.e new areas in extremes! Strict accordance with the 416 records used in this study was carried in! Dermacentor species and Haemaphysalis species have also been implicated cells and that are associated with several diseases! Expansions to take place [ 45 ] a vector in Europe and elevational of. Dis 5 ( 5 ): e1186 [ 23 ] available via Figshare repository ( https: //doi.org/10.1371/journal.pone.0189092.s004,:... Same vectors [ 12 ] and later shown to inhibit T-cell activation from this.... In Morocco, Algeria, and molted nymphs were not tested due to B.. Models ( dark red represents high average and dark blue represents areas with frequent... Scholar ; Cotté V, Bonnet S Le Rhun D et al cell! Obtained in our previous study [ 11 ] and immunofluorecence assay on 100 µl of the and.