AGW Observer

Observations of anthropogenic global warming

Papers on ticks and global warming

Posted by Ari Jokimäki on August 11, 2011

This is a list of papers on global warming effects on tick populations and the diseases they spread. The list is not complete, and will most likely be updated in the future in order to make it more thorough and more representative.

UPDATE (September 12, 2011): Beugnet & Marié (2009), Dautel et al. (2006), Bullová et al. (2009), Dantas-Torres (2010), and Gern et al. (2008) added.

Modelling the effects of recent changes in climate, host density and acaricide treatments on population dynamics of Ixodes ricinus in the UK – Dobson & Randolph (2011) “A population model for the tick Ixodes ricinus, the most significant vector of pathogens in Europe, is used to explore the relative impact of changes in climate, host density and acaricide-treated hosts on tick abundance and seasonality. A rise in temperature of the sort witnessed since 1989 speeds up the inter-stadial development of ticks, thereby reducing the cumulative effect of constant daily mortality rates and potentially raising population levels. The predicted earlier onset of tick-questing activity in the spring, due to stage-specific temperature thresholds, could increase contact between ticks and humans during recreational visits to the countryside in spring holidays. These tick population effects vary geographically with background climate. The significant increase in deer abundance across Europe, including the UK, in recent decades is predicted to drive tick population increases, the effect varying with the initial density of hosts. In areas only recently colonized by deer, tick numbers are predicted to rise dramatically (given suitable climatic conditions). Where host densities are already high, however, further increases may reduce numbers of questing ticks; unfed ticks leave the questing population more rapidly, even though the overall tick population (and therefore pathogen transmission potential) increases. Culling high-density deer populations as a control measure could, therefore, initially cause an apparent increase in questing ticks, with the predicted long-term population trajectory depending on the severity of the cull. Conversely, the further addition of large hosts (e.g. sheep) would effectively reduce the number of questing ticks and therefore the risk to humans. If such sheep were treated with acaricide, tick populations are predicted to decrease rapidly, to an extent that depends on the relative abundance of wild (untreated) and treated hosts. Tick control in designated areas may be achieved by using sheep in this way as ‘lethal mops’, as used to occur in the past when sheep were regularly dipped. Synthesis and applications: Both abiotic and biotic environmental changes witnessed recently could have contributed to apparent increases in tick populations, especially where these environmental factors were limiting in the past. The release of additional hosts treated with long-lasting acaricide is potentially an effective control strategy.” Andrew D. M. Dobson, Sarah E. Randolph, Journal of Applied Ecology, Volume 48, Issue 4, pages 1029–1037, August 2011, DOI: 10.1111/j.1365-2664.2011.02004.x.

Mathematical modelling of the impact of climatic conditions in France on Rhipicephalus sanguineus tick activity and density since 1960 – Beugnet et al. (2011) “Rhipicephalus sanguineus, the brown dog tick, has a worldwide distribution in areas with a relatively warm climate, including mild winters. This tick plays an important role as vector for various animal and human pathogens, including bacteria and protozoa. Based on precise daily meteorological data from the past 40 years, combined with mathematical modelling designed to predict tick activity, two modelling approaches were developed. The first examined the evolution of the number of weeks with favourable biological conditions for ticks in four French cities located at various latitudes of the country: Nîmes in the south, Paris in the north, Lyon in the east and Nantes in the west. The second analysed the extension of the geographical surface area in km(2) where the biological conditions favour tick activity for at least 12 weeks per year. Both analyses revealed clear evidence of increased temperatures coupled with an augmented tick activity index in three of the four cities. However, the change was not significant in Nîmes, where the climate is Mediterranean and the tick is already endemic. For Paris, Lyon and Nantes, the activity index values have increased significantly, i.e. by 4.4%, 4.0% and 3.4%, respectively. The distribution of the activity index values is evolving strongly with significantly fewer values below 50% since the 1960s and a clear decrease of values between 20% and 50% during the latest decade. Between 1960 and 2000, the theoretical extension of the surface area where the climatic index is suitable for R. sanguineus has increased by 66%. Even though several other important factors, such as changes in biotopes or human activity, are not included in this study, the resulting patterns and trends are noticeable. Our models constitute the first demonstration of the impact of climate change on the activity and distribution of ticks and confirm the observed northward migration trend for this Mediterranean domestic tick.” Beugnet F, Kolasinski M, Michelangeli PA, Vienne J, Loukos H., Geospat Health. 2011 May;5(2):255-63. [Full text]

A clear and present danger: tick-borne diseases in Europe – Heyman et al. (2010) “Ticks can transmit a variety of viruses, bacteria or parasites that can cause serious infections or conditions in humans and animals. While tick-borne diseases are becoming an increasing and serious problem in Europe, tick-borne diseases are also responsible for major depressions in livestock production and mortality in sub-Saharan Africa, Latin America and Asia. This review will focus on the most important circulating tick-transmitted pathogens in Europe (Borrelia spp., Anaplasma phagocytophilum, Babesia spp., tick-borne encephalitis virus, Rickettsia spp. and Crimean-Congo hemorrhagic fever virus).” Heyman, Paul, Cochez, Christel, Hofhuis, Agnetha, van der Giessen, Joke, Sprong, Hein, Porter, Sarah Rebecca, Losson, Bertrand, Saegerman, Claude, Donoso-Mantke, Oliver, Niedrig, Matthias, Papa, Anna, Expert Review of Anti-Infective Therapy, Volume 8, Number 1, January 2010, pp. 33-50(18).

Biology and ecology of the brown dog tick, Rhipicephalus sanguineus – Dantas-Torres (2010) “The brown dog tick (Rhipicephalus sanguineus) is the most widespread tick in the world and a well-recognized vector of many pathogens affecting dogs and occasionally humans. This tick can be found on dogs living in both urban and rural areas, being highly adapted to live within human dwellings and being active throughout the year not only in tropical and subtropical regions, but also in some temperate areas. Depending on factors such as climate and host availability, Rh. sanguineus can complete up to four generations per year. Recent studies have demonstrated that ticks exposed to high temperatures attach and feed on humans and rabbits more rapidly. This observation suggests that the risk of human parasitism by Rh. sanguineus could increase in areas experiencing warmer and/or longer summers, consequently increasing the risk of transmission of zoonotic agents (e.g., Rickettsia conorii and Rickettsia rickettsii). In the present article, some aspects of the biology and ecology of Rh. sanguineus ticks are discussed including the possible impact of current climate changes on populations of this tick around the world.” Filipe Dantas-Torres, Parasites & Vectors, Volume 3, Number 1, 26, DOI: 10.1186/1756-3305-3-26. [Full text]

To what extent has climate change contributed to the recent epidemiology of tick-borne diseases? – Randolph (2010) “There is no doubt that all vector-borne diseases are very sensitive to climatic conditions. Many such diseases have shown marked increases in both distribution and incidence during the past few decades, just as human-induced climate change is thought to have exceeded random fluctuations. This coincidence has led to the general perception that climate change has driven disease emergence, but climate change is the inevitable backdrop for all recent events, without implying causality. Coincidence and causality can be disentangled using tick-borne encephalitis (TBE) as a test case, based on the excellent long-term data for this medically significant European disease system. Detailed analysis of climate records since 1970 has revealed abrupt temperature increases just prior to the dramatic upsurge in TBE incidence in many parts of central and eastern Europe. Furthermore, the seasonal patterns of this temperature change are such as might have favoured the transmission of TBE virus between co-feeding ticks. Nevertheless, the pattern of climate change is too uniform to explain the marked heterogeneity in the timing and degree of TBE upsurge, for example in different counties within each of the Baltic countries. Recent decreases as well as increases in TBE incidence must also be taken into account. Instead of a single cause, a network of interacting factors, acting synergistically but with differential force in space and time, would generate this epidemiological heterogeneity. From analysis of past and present events, it appears that human behavioural factors have played a more significant role than purely biological enzootic factors, although there is an explicit causal linkage from one to the other. This includes a range of abiotic and biotic environmental factors, together with human behaviour determined by socio-economic conditions. Many of the abrupt changes followed from the shift from planned to market economies with the fall of Soviet rule. Comparisons between eight countries have indeed revealed a remarkable correlation between poverty indicators and the relative degree of upsurge in TBE from 1993. Against this background of longer-term shifts in TBE incidence, sudden spikes in incidence appear to be due to exceptional weather conditions affecting people’s behaviour, which have a differential impact depending on socio-economic factors. This new perspective may also help explain the epidemiology of Crimean-Congo haemorrhagic fever around the eastern Mediterranean region, including the current exceptional epidemic in Turkey.” Sarah E. Randolph, Veterinary Parasitology, Volume 167, Issues 2-4, 10 February 2010, Pages 92-94, doi:10.1016/j.vetpar.2009.09.011.

Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? – Gilbert (2010) “The impact of climate change on vector-borne infectious diseases is currently controversial. In Europe the primary arthropod vectors of zoonotic diseases are ticks, which transmit Borrelia burgdorferi sensu lato (the agent of Lyme disease), tick-borne encephalitis virus and louping ill virus between humans, livestock and wildlife. Ixodes ricinus ticks and reported tick-borne disease cases are currently increasing in the UK. Theories for this include climate change and increasing host abundance. This study aimed to test how I. ricinus tick abundance might be influenced by climate change in Scotland by using altitudinal gradients as a proxy, while also taking into account the effects of hosts, vegetation and weather effects. It was predicted that tick abundance would be higher at lower altitudes (i.e. warmer climates) and increase with host abundance. Surveys were conducted on nine hills in Scotland, all of open moorland habitat. Tick abundance was positively associated with deer abundance, but even after taking this into account, there was a strong negative association of ticks with altitude. This was probably a real climate effect, with temperature (and humidity, i.e. saturation deficit) most likely playing an important role. It could be inferred that ticks may become more abundant at higher altitudes in response to climate warming. This has potential implications for pathogen prevalence such as louping ill virus if tick numbers increase at elevations where competent transmission hosts (red grouse Lagopus lagopus scoticus and mountain hares Lepus timidus) occur in higher numbers.” Lucy Gilbert, Oecologia, Volume 162, Number 1, 217-225, DOI: 10.1007/s00442-009-1430-x.

Effects of Climate Change on Ticks and Tick-Borne Diseases in Europe – Gray et al. (2009) “Zoonotic tick-borne diseases are an increasing health burden in Europe and there is speculation that this is partly due to climate change affecting vector biology and disease transmission. Data on the vector tick Ixodes ricinus suggest that an extension of its northern and altitude range has been accompanied by an increased prevalence of tick-borne encephalitis. Climate change may also be partly responsible for the change in distribution of Dermacentor reticulatus. Increased winter activity of  I. ricinus is probably due to warmer winters and a retrospective study suggests that hotter summers will change the dynamics and pattern of seasonal activity, resulting in the bulk of the tick population becoming active in the latter part of the year. Climate suitability models predict that eight important tick species are likely to establish more northern permanent populations in a climate-warming scenario. However, the complex ecology and epidemiology of such tick-borne diseases as Lyme borreliosis and tick-borne encephalitis make it difficult to implicate climate change as the main cause of their increasing prevalence. Climate change models are required that take account of the dynamic biological processes involved in vector abundance and pathogen transmission in order to predict future tick-borne disease scenarios.” J. S. Gray, H. Dautel, A. Estrada-Peña, O. Kahl, and E. Lindgren, Interdisciplinary Perspectives on Infectious DiseasesVolume 2009 (2009), Article ID 593232, 12 pages, doi:10.1155/2009/593232. [Full text]

Spatial distribution of Dermacentor reticulatus tick in Slovakia in the beginning of the 21st century – Bullová et al. (2009) “A new field survey monitoring the spatial distribution of Dermacentor (D.) reticulatus (Fabricius, 1794) tick in Slovakia was carried out in 2005–2008 in order to record changes in its distribution when compared to former studies. Last surveys on the geographical distribution were conducted in 1950s and 1970s and the presence of D. reticulatus was determined along the rivers in the south-east (Latorica) as well as in the south-west (Morava, Dunaj) Slovakia. In the present survey new areas with D. reticulatus occurrence were detected, providing evidence that this tick species has extended its range in the surroundings of its former habitats but also by at least 200 km further North and by 300 m of elevation into higher altitudes. D. reticulatus is known to transmit Babesia spp. causing babesiosis in cattle and dogs. Expansion of D. reticulatus range is therefore likely to bring a spread of babesiosis, which can be severe or fatal especially for dogs.” Eva Bullová, Martin Lukáň, Michal Stanko, Branislav Peťko, Veterinary Parasitology, Volume 165, Issues 3-4, 12 November 2009, Pages 357-360, doi:10.1016/j.vetpar.2009.07.023.

Emerging arthropod-borne diseases of companion animals in Europe – Beugnet & Marié (2009) “Vector-borne diseases are caused by parasites, bacteria or viruses transmitted by the bite of hematophagous arthropods (mainly ticks and mosquitoes). The past few years have seen the emergence of new diseases, or re-emergence of existing ones, usually with changes in their epidemiology (i.e. geographical distribution, prevalence, and pathogenicity). The frequency of some vector-borne diseases of pets is increasing in Europe, i.e. canine babesiosis, granulocytic anaplasmosis, canine monocytic ehrlichiosis, thrombocytic anaplasmosis, and leishmaniosis. Except for the last, these diseases are transmitted by ticks. Both the distribution and abundance of the three main tick species, Rhipicephalus sanguineus, Dermacentor reticulatus and Ixodes ricinus are changing. The conditions for such changes involve primarily human factors, such as travel with pets, changes in human habitats, social and leisure activities, but climate changes also have a direct impact on arthropod vectors (abundance, geographical distribution, and vectorial capacity). Besides the most known diseases, attention should be kept on tick-borne encephalitis, which seems to be increasing in western Europe, as well as flea-borne diseases like the flea-transmitted rickettsiosis. Here, after consideration of the main reasons for changes in tick vector ecology, an overview of each “emerging” vector-borne diseases of pets is presented.” Frederic Beugnet, Jean-Lou Marié, Veterinary Parasitology, Volume 163, Issue 4, 26 August 2009, Pages 298-305, doi:10.1016/j.vetpar.2009.03.028. [Full text]

Influence of some climatic factors on Ixodes ricinus ticks studied along altitudinal gradients in two geographic regions in Switzerland – Gern et al. (2008) “In the context of climate change, the seasonal activity of questing Ixodes ricinus and their infection with Borrelia burgdorferi sensu lato (s.l.) were examined in relation to some climatic data along altitudinal gradients in Switzerland. The first study took place in an Alpine area (Valais) from 750 to 1020 m above sea level. The other gradient was located on a mountain in the foothills of the Jura chain (Neuchâtel) from 620 to 1070 m above sea level. In the Alpine area, the highest questing tick density was observed at the highest altitude. At the lowest altitudes (750 and 880 m), very high saturation deficits, >10 mmHg, were present during most of the tick activity season and they seem to have impaired the thriving of tick populations. The second study in Neuchâtel (2003–2005) was a follow-up of a previous study (1999–2001) in which it was observed that tick density decreased with increasing altitude. During the follow-up study, substantial differences in questing tick density and phenology of ticks were observed: At high elevations, questing tick densities were 2.25 and 3.5 times higher for nymphs and adults, respectively, than during 1999–2001. As observed during 1999–2001, questing tick density decreased with increasing altitude in this site in 2003–2005. Tick questing density remained higher at the lowest altitude. Increased temperatures during summer months, more favorable for ticks, reaching values similar to those registered in the first study at the lowest elevations are probably responsible for the higher tick questing density at high altitudes. B. burgdorferi s.l. infection prevalence in ticks decreased with increasing altitudes along both altitudinal gradients. Long-lasting high saturation deficit values may limit the development of tick populations as too high a moisture stress has a negative effect on tick survival. This factor may have a permanent impact, as it is probably the case at the lowest altitudes in the Alpine area or a more transient effect like in the Neuchâtel gradient.” Lise Gern, Francisca Morán Cadenas, Caroline Burri, International Journal of Medical Microbiology, Volume 298, Supplement 1, 1 September 2008, Pages 55-59, doi:10.1016/j.ijmm.2008.01.005. [Full text]

Ixodes ricinus seasonal activity: Implications of global warming indicated by revisiting tick and weather data – Gray (2008) “A recent climate experiment predicted that average maximum summer temperatures in southern regions of the British Isles may approach 30 °C by the year 2020. An opportunity for retrospective analysis of the implications of such a change for tick phenology and disease transmission was presented by the coincidence of unusually high early summer temperatures in 1976 with the collection of tick data from sites in Ireland where host availability was controlled. Subsequent identification of diapause threshold periods and simulation of temperature-dependent tick development showed that high summer temperatures can cause mass transfer of ticks between development cohorts, resulting in increased activity and therefore increased disease transmission in late autumn and early spring. This suggests that in northern temperate regions of Europe global warming is likely to cause changes in the seasonal patterns of tick-borne diseases.” Jeremy S. Gray, International Journal of Medical Microbiology, Volume 298, Supplement 1, 1 September 2008, Pages 19-24, doi:10.1016/j.ijmm.2007.09.005.

Evidence for an increased geographical distribution of Dermacentor reticulatus in Germany and detection of Rickettsia sp. RpA4 – Dautel et al. (2006) “Two studies were performed to elucidate the current distribution of the tick Dermacentor reticulatus in Germany. In the first one in 2003, a total of 365 dogs from 171 sites in the states of Berlin and Brandenburg was screened for ticks, and the corresponding outdoor sites that the dogs usually visited were searched for host-seeking ticks by the flagging method. A total of 1155 ticks was removed from the dogs. The majority were Ixodes ricinus (88.5%), followed by D. reticulatus (9.1%) and I. hexagonus (2.4%). Altogether, 222 dogs carried I. ricinus (60.8%), 41 D. reticulatus (11.2%) and 15 I. hexagonus (4.1%) ticks. Based on scutal index determination, the removed I. ricinus and D. reticulatus had been feeding on the dogs for a mean of 4.0 and 4.5 days, respectively. The dogs infested with D. reticulatus lived at 26 different sites, all previously unknown as Dermacentor sites. Seven of the sites could be confirmed subsequently by flagging the vegetation for ticks. In the second study, a total of 721 deer was shot at 201 different sites from a total of 160 districts all over Germany during the autumn hunting season 2004. A total of 23 deer (3.2%) originating from 14 sites was infested with D. reticulatus. Hereby, significantly more red deer (Cervus elaphus elaphus) than roe deer (Capreolus capreolus) or fallow deer (Dama dama) harboured D. reticulatus ticks. Only two of the sites found had already been known as D. reticulatus areas, whereas all other sites in Brandenburg, Saxony Anhalt, Hesse and Bavaria had been unknown. The results of both studies show that D. reticulatus presently occurs at far more sites than previously known in Germany and thus most likely has expanded its range. Additionally, a total of 135 D. reticulatus removed from deer was screened for Babesia canis and Rickettsia sp. by PCR. A total of 31 D. reticulatus (23%) were positive for Rickettsia. Sequencing revealed in all cases 100% identity with the strain RpA4 that was first isolated from Rhipicephalus ticks in Russia.” Hans Dautel, Cornelia Dippel, Rainer Oehme, Kathrin Hartelt, Elvira Schettler, International Journal of Medical Microbiology, Volume 296, Supplement 1, 22 May 2006, Pages 149-156, doi:10.1016/j.ijmm.2006.01.013.

A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis – Ogden et al. (2005) “A dynamic population model of Ixodes scapularis, the vector of a number of tick-borne zoonoses in North America, was developed to simulate effects of temperature on tick survival and seasonality. Tick development rates were modelled as temperature-dependent time delays, calculated using mean monthly normal temperature data from specific meteorological stations. Temperature also influenced host-finding success in the model. Using data from stations near endemic populations of I. scapularis, the model reached repeatable, stable, cyclical equilibria with seasonal activity of different instars being very close to that observed in the field. In simulations run using data from meteorological stations in central and eastern Canada, the maximum equilibrium numbers of ticks declined the further north was the station location, and simulated populations died out at more northerly stations. Tick die-out at northern latitudes was due to a steady increase in mortality of all life stages with decreasing temperature rather than a specific threshold event in phenology of one life stage. By linear regression we investigated mean annual numbers of degree-days >0 °C (DD>0 °C) as a readily mapped index of the temperature conditions at the meteorological stations providing temperature data for the model. Maximum numbers of ticks at equilibrium were strongly associated with the mean DD>0 °C (r2>0.96, POntario, β=103, P<0.001). The intercepts of the regression models provided theoretical limits for the establishment of I. scapularis in Canada. Maps of these limits suggested that the range of southeast Canada where temperature conditions are currently suitable for the tick, is much wider than the existing distribution of I. scapularis, implying that there is potential for spread. Future applications of the model in investigating climate change effects on I. scapularis are discussed." N.H. Ogden, M. Bigras-Poulin, C.J. O’Callaghan, I.K. Barker, L.R. Lindsay, A. Maarouf, K.E. Smoyer-Tomic, D. Waltner-Toews and D. Charron, International Journal for Parasitology, Volume 35, Issue 4, 1 April 2005, Pages 375-389, doi:10.1016/j.ijpara.2004.12.013. [Full text]

Evidence that climate change has caused ‘emergence’ of tick-borne diseases in Europe? – Randolph (2004) “Even though tick-borne disease systems are highly susceptible to climatic influences, climate change to date is not necessarily the cause of the marked increased incidence of a variety of tick-borne diseases in many parts of Europe over the past two decades. To test for causality, rather than coincidence, we need to examine whether the right sorts of climate change have occurred at the right time and in the right places to account for the observed heterogeneous temporal and spatial patterns of tick-borne disease ‘emergence’. Tick-borne encephalitis (TBE) incidence, for example, showed a 3-fold step increase from 1983 to 1986 in Sweden, doubled in 1993 in the Czech Republic, increased even more dramatically in the same year in Lithuania and Poland, but declined markedly in 1997 in Hungary, Croatia and Slovenia. Within each country, TBE incidence has changed to different degrees in different regions. Because other tick-borne diseases, notably Lyme borreliosis, has commonly ‘emerged’ in parallel with TBE, we should first examine climate variables predicted to have a general effect on tick abundance, which has indeed increased in the past decade. These include temperature and moisture stress, which have seasonally differential impacts. Monthly mean records for 1960–2000 from the UK Climate Research Unit’s interpolated global climate surface reveal that mean spring, spring-autumn and winter temperatures have all increased gradually over the past 40 years, but apparently most sharply in the late 1980s, when moisture stress also increased. These climate data do not reveal any obvious differences between sites where TBE did or did not ‘emerge’, and in Sweden increases in TBE pre-dated the onset of warmer springs and winters. If recorded climate changes cannot yet satisfactorily explain the temporal and spatial patterns of tick-borne disease change in Europe, the impact of biotic factors, such as increases in deer abundance and changing habitat structure, and of socio-political changes following the end of communist rule, demand more detailed quantitative analyses.” Sarah E. Randolph, International Journal of Medical Microbiology Supplements, Volume 293, Supplement 37, April 2004, Pages 5-15, doi:10.1016/S1433-1128(04)80004-4.

A tick-borne encephalitis ceiling in Central Europe has moved upwards during the last 30 years: Possible impact of global warming? – Zeman & Beneš (2004) “The geographic/temporal pattern of cases of tick-borne encephalitis (TBE) registered in the Czech Republic since 1970 was analysed to verify the surmise of a global warming effect. Using a geographic information system, over 8,700 notified places of infection were pinpointed on a map and overlaid with a digital elevation model to estimate the vertical distribution of the cases. Series of yearly disease ceilings (assessed alternatively as the respective maximum altitude or mean altitudes of the upper 5 or 10 cases) were tested against the null hypothesis of random elevation course and analysed for correlation with concomitant factors (yearly TBE incidence rate, mean yearly temperature, population density of small rodents and roe deer). Statistical tests proved that the TBE ceiling has gradually moved upwards in the course of the last three decades. The average rate of ascension within this period was approx. 5.4 ± 1.7 m yearly, which corresponds well with concurrent mean temperature rising of approx. 0.036 ± 0.007°C yearly, and the vertical temperature gradient of 0.0065 ± 0.0004°C m−1. The TBE-ceiling estimates significantly correlated with TBE-incidence data and the mean yearly temperature recorded 1–2 years earlier. Although TBE incidence correlated with rodent population density that was observed 1–2 years earlier, the TBE ceiling does not seem to be influenced by rodent population dynamics nor did the population dynamics correlate with mean yearly temperatures. TBE incidence as well as mean altitudes of the upper 10 cases also correlated with official data on harvested roe deer. Overall, the fluctuations of TBE incidence and TBE ceiling proved to be synchronous processes that correspond with temperature changes. Although the dependence of TBE on temperature is not a direct one and various factors could be involved, an impact of climate warming on the vertical disease distribution in Central Europe is evident.” Petr Zemana and Cestmir Beneš, International Journal of Medical Microbiology Supplements, Volume 293, Supplement 37, April 2004, Pages 48-54, doi:10.1016/S1433-1128(04)80008-1.

Shift of the Tick Ixodes ricinus and Tick-Borne Encephalitis to Higher Altitudes in Central Europe – Daniel et al. (2003) No abstract. M. Daniel, V. Danielová, B. Kříž, A. Jirsa and J. Nožička, European Journal of Clinical Microbiology & Infectious Diseases, Volume 22, Number 5, 327-328, DOI: 10.1007/s10096-003-0918-2.

Tick-borne encephalitis in Sweden and climate change – Lindgren & Gustafson (2001) “Background: The incidence of tick-borne encephalitis (TBE) in Sweden has substantially increased since the mid-1980s. During the same period the climate has become milder and ticks have become more abundant. We investigated whether there is a link between the change in climate and the increase in incidence of TBE. Methods: Since the late 1950s all cases of encephalitis admitted in Stockholm County have been serologically tested for TBE. We analysed the period 1960–98 with multiple regressions. The number of days per season with temperatures of known importance for tick prevalence and pathogen transmission were studied. 2 years of temperature data were related to each TBE incidence rate to account for the tick’s long life-span. Findings: Increases in disease incidence was significantly related (R2=0·58; p<0·0001) to a combination of two consecutive mild winters, temperatures favouring spring development (8–10°C) and extended autumn activity (5–8°C) in the year prior to the incidence year, and temperatures allowing tick activity (5–8°C) early in the incidence year. Interpretations: The findings indicate that the increase in TBE incidence since the mid-1980s is related to the period's change towards milder winters and early arrival of spring. Other factors may have influenced TBE incidence such as more people in endemic locations, and increases in host animal populations; factors which are partly climate related. Access to TBE vaccination since 1986 and increased awareness of ticks might have caused an underestimation of the links found. Our findings also suggest that the incidence of other tick-borne zoonoses might have been affected by the milder climate." Elisabet Lindgren and Rolf Gustafson, The Lancet, Volume 358, Issue 9275, 7 July 2001, Pages 16-18, doi:10.1016/S0140-6736(00)05250-8. [Full text]

Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change – Randolph & Rogers (2000) “Repeated predictions that vector–borne disease prevalence will increase with global warming are usually based on univariate models. Toaccommodate the full range of constraints, the present–day distribution of tick–borne encephalitis virus (TBEv) was matched statistically to current climatic variables, to provide a multivariate description of present–day areas of disease risk. This was then applied to outputs of a general circulation model that predicts how climatic variables may change in the future, and future distributions of TBEv were predicted for them. The expected summer rise in temperature and decrease in moisture appears to drive the distribution of TBEv into higher–latitude and higher–altitude regions progressively through the 2020s, 2050s and 2080s. The final toe–hold in the 2080s may be confined to a small part of Scandinavia, including new foci in southern Finland. The reason for this apparent contraction of the range of TBEv is that its transmission cycles depend on a particular pattern of tick seasonal dynamics, which may be disrupted by climate change. The observed marked increase in incidence of tick–borne encephalitis in most parts of Europe since 1993 may be due to non–biological causes, such as political and sociological changes.” Sarah E. Randolph and David J. Rogers, Proc. R. Soc. Lond. B 7 September 2000 vol. 267 no. 1454 1741-1744, doi: 10.1098/rspb.2000.1204. [Full text]

Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus – Lindgren et al. (2000) “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.” E Lindgren, L Tälleklint, and T Polfeldt, Environ Health Perspect. 2000 February; 108(2): 119–123. [Full text]

Seasonal synchrony: the key to tick-borne encephalitis foci identified by satellite data – Randolph et al. (2000) “A previous analysis of tick infestation patterns on rodents in Slovakia suggested that the key to the focal distribution of western-type tick-borne encephalitis virus (TBEv) in Europe is the geographically variable degree of synchrony in the seasonal activity of larval and nymphal Ixodes ricinus ticks. This prediction is here tested by examining records, from 7 different countries, of the seasonal variation in the abundance of larvae and nymphs feeding on rodents or questing on the vegetation. Larvae consistently started feeding and questing earlier in the year at sites within TBEv foci than elsewhere, so that they appeared in the spring as soon as nymphs were active. Such larval–nymphal synchrony is associated with a rapid fall in ground-level temperatures from August to October as revealed by the satellite-derived index of Land Surface Temperature (LST). Likewise, of 1992 pixels sampled on a grid across Europe, the 418 that fell within TBEv foci were characterized by a higher than average rate of autumnal cooling relative to the peak midsummer LST. It is proposed that such a seasonal temperature profile may cause unfed larvae to pass the winter in quiescence, from which they emerge synchronously with nymphs in the spring.” S. E. Randolph, R. M. Green, M. F. Peacey and D. J. Rogers, Parasitology, 2000, 121: 15-23. [Full text]

Ticks and tick-borne disease systems in space and from space – Randolph (2000) “Analyses within geographical information systems (GISs) indicate that small- and large-scale ranges of hard tick species (Ixodidae) are determined more by climate and vegetation than by host-related factors. Spatial distributions of ticks may therefore be analysed by statistical methods that seek correlations between known tick presence/absence and ground- or remotely-sensed (RS) environmental factors. In this way, local habitats of Amblyomma variegatum in the Caribbean and Ixodes ricinus in Europe have been mapped using Landsat RS imagery, while regional and continental distributions of African and temperate tick species have been predicted using multi-temporal information from the National Oceanic and Atmospheric Administration-Advanced Very High Resolution Radiometer (NOAA-AVHRR) imagery. These studies illustrate ways of maximizing statistical accuracy, whose interpretation is then discussed in a biological framework. Methods such as discriminant analysis are biologically transparent and interpretable, while others, such as logistic regression and tree-based classifications, are less so. Furthermore, the most consistently significant variable for predicting tick distributions, the RS Normalized Difference Vegetation Index (NDVI), has a sound biological basis in that it is related to moisture availability to free-living ticks and correlated with tick mortality rates. The development of biological process-based models for predicting the spatial dynamics of ticks is a top priority, especially as the risk of tick-borne infections is commonly related not simply to the vector’s density, but to its seasonal population dynamics. Nevertheless, using statistical pattern-matching, the combination of RS temperature indices and NDVI successfully predicts certain temporal features essential for the transmission of tick-borne encephalitis virus, which translate into a spatial pattern of disease foci on a continental scale.” S.E. Randolph, Advances in Parasitology, Volume 47, 2000, Pages 217-243, Remote Sensing and Geographical Information Systems in Epidemiology, doi:10.1016/S0065-308X(00)47010-7.

Climate and Tickborne Encephalitis – Lindgren (2000) “Climatic changes are projected to alter the abundance, dynamics, and geographical distribution of many vector-borne diseases in human populations. Tick-borne diseases such as Lyme disease and tick-borne encephalitis (TBE) are a growing concern in northern Europe and the United States. The impact of a future climate change on the transmission of tick-borne diseases is not known. To make such assumptions, more empirical data are needed on the relations between short-term fluctuations in contemporary weather and disease incidence. This paper analyzes relations between daily minimum and maximum temperatures, monthly precipitation, and TBE incidence during a 36-yr period in Stockholm County, a high-endemic region for TBE in Sweden. Multiple regression analyses were performed, with temperature variables expressed as number of days per winter or spring – summer – fall season with temperatures above, below, or in the interval between different temperature limits. The limits used for daily minimum temperatures represent bioclimatic thresholds of importance for pathogen transmission. To adjust for the length of the tick’s life cycle, each TBE incidence rate was related to meteorological data over two consecutive years. Results reveal that increased incidence of tick-borne encephalitis is related to a combination of two successive years of more days with temperatures permitting prolonged seasonal tick activity and, hence, pathogen transmission (i.e., daily minimum temperatures above 5ºC-10ºC), and a mild winter preceding the year before the incidence year (i.e., fewer winter days with minimum temperatures below -7ºC). Alternative explanations of the results are discussed. Findings of this study suggest that a climate change may extend the seasonal range and intensify the endemicity of tick-borne diseases, in particular, at northern latitudes.” Elisabet Lindgren. 1998, Conservation Ecology [online] 2(1): 5.. [Full text]

Climate change, tick-borne encephalitis and vaccination needs in Sweden—a prediction model – Lindgren (1998) “A future, global, climate change may indirectly lead to changes in the transmission and incidence of several vector-borne diseases. This paper presents an example of a modeling tool for projections of possible changes in the incidence of tick-borne encephalitis (TBE), and the subsequent changes in vaccination needs, during the next half-century in Sweden. The model is based on the Hadley Center’s regional temperature predictions for the year 2050, taking into account the IPCC IS92 ‘non-intervention scenario’. The model has been constructed into STELLA, a graphical dynamic-simulation, soft-ware program. The model project an increase in TBE incidence in Stockholm County, a high-endemic region in Sweden, during the next 50 years. According to this simplified model, the annual vaccination rate need to increase by 3–4-fold during the next half century in order to prevent the projected increases in TBE incidence in the region from a climatic change.” Elisabet Lindgren, Ecological Modelling, Volume 110, Issue 1, 1 July 1998, Pages 55-63, doi:10.1016/S0304-3800(98)00041-6. [Full text]

Increasing Geographical Distribution and Density of Ixodes ricinus (Acari: Ixodidae) in Central and Northern Sweden – Tälleklint & Jaenson (1998) “The geographical distribution and density of Ixodes ricinus (L.) in the 2 northern regions, Svealand and Norrland, in Sweden were studied by using a questionnaire in Swedish magazines for house owners and dog owners, and in provincial newspapers. Analysis of the ≍1,200 answers revealed that ticks are present in all parts of Svealand (except northern Varmland and northern and western Dalarna), the southeastern part of Norrland (i.e., Gästrikland and Hälsingland), and along the Baltic Sea coast of central and northern Norrland. The proportion of answers reporting ticks and the estimated tick density (i.e., the number of ticks infesting dogs and cats) decreased from south to north. The answers to the questionnaire and data from field sampling of ticks suggest that tick density decreased distinctly along a narrow boundary zone, coinciding with the biological limit of Norrland (Limes Norrlandicus), crossing Sweden through southern Varmland, southeastern Dalarna, and central Gastrikland. The results of the questionnaire suggest that I. ricinus ticks are more widespread today than in the early 1980s, especially in Varmland, western and central Dalarna, Hiilsingland, and the coastal areas of Medelpad, Angermanland, and Vasterbotten, and that the proportion of the human population at risk for tick-borne pathogens in Svealand and Norrland is increasing.” Tälleklint, Lars; Jaenson, Thomas G. T., Journal of Medical Entomology, Volume 35, Number 4, July 1998 , pp. 521-526(6).

Geographical Distribution, Host Associations, and Vector Roles of Ticks (Acari: Ixodidae, Argasidae) in Sweden – Jaenson et al. (1994) “This review covers the geographic distribution and host relationships of the tick species in Sweden. Ixodes uriae White, I. caledonicus Nuttall, I. unicavatus Neumann, I. arboricola Schulze & Schlottke, and I. lividus Koch are ornithophagous species. I. trianguliceps Birula, I. canisuga Johnston, I. hexagonus Leach, and Argas vespertilionis (Latreille) are mammalophagous. I. ricinus (L.) and Haemaphysails punctata Canestrini & Fanzago feed on both birds and mammals. All these tick species may be considered to be permanently present in Sweden. I. persulcatus Schulze, Hyalomma marginatum Koch, and the brown dog tick, Rhipicephalus satiguineus (Latreille), may be regarded as not indigenous to Sweden although they may be regularly introduced by spring-migrating birds or imported dogs, respectively. The first European record of the American dog tick, Dermacentor variabilis (Say), is reported. There are several records of Hyalomma aegyptium (L.) from imported tortoises in Sweden. Excluding other ticks imported on exotic pets and zoo animals, another 13 tick species are listed that may occur, at least occasionally, in Sweden. Because of its wide geographic distribution, great abundance, and wide host range, I. ricinus is medically the most important arthropod in northern Europe. I. ricinus is common in southern and south-central Sweden and along the coast of northern Sweden and has been recorded from 29 mammal species, 56 bird species, and two species of lizards in Sweden alone. The potential introduction to Sweden of exotic pathogens with infected ticks (e.g., I. persulcatus and H. marginatum on birds or Dermacentor spp. and R. sanguineus on mammals) is evident.” Jaenson, Thomas G. T., Tälleklint, Lars, Lundqvist, Lars, Olsen, Björn, Chirico, Jan, Mejlon, Hans, Journal of Medical Entomology, Volume 31, Number 2, March 1994 , pp. 240-256(17).


One Response to “Papers on ticks and global warming”

  1. Ari Jokimäki said

    I added Beugnet & Marié (2009), Dautel et al. (2006), Bullová et al. (2009), Dantas-Torres (2010), and Gern et al. (2008).

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