The impacts of climate and land use change on tick-related risks
It is widely accepted that the range of many tick species is expanding due to global warming, host-animal migration, and land fragmentation through deforestation and urbanization of natural continuous forests into smaller sections.1-4 Climate projections show that ticks are increasing their range northwards by 35–55 km per year.3 Tick species are known arthropod vectors, and can transmit a wide range of bacterial, viral, and protozoan pathogens to both humans and other animal species.5,6 As the range of tick vectors increases across Canada, so does the potential for exposure to emerging tick-borne pathogens. The aim of this document is to review environmental factors that contribute to tick-related risks. This is the second document in a four-part series focussing on the risks of tick exposure in Canada. The first review entitled “A review of ticks in Canada and health risks from exposure” can be found here.
Literature search methodology
Scholarly research and grey literature were searched for information on ticks, climate change, land use change, forest fragmentation, and environmental ecology. Databases to identify relevant sources include Web of Science, PubMed, and Google Scholar. Grey literature and reports from academic institutions and governments were also reviewed. Relevant English language results were compiled. Although the search was primarily restricted to 2000–present, some earlier pivotal publications were included. Forward and backward chaining of initial results identified additional references.
Articles, reports, and websites were selected for review if they pertained to ticks and at least one of the following: climate change, land use change, forest fragmentation and/or environmental ecology. Both the common name and Latin name of pathogens and of known tick vectors were included in the search. The majority of the literature focussed on areas in the United States where ticks have been endemic for much longer time periods. Where possible, literature pertaining to Canada’s provinces and territories was emphasized. The literature was also predominantly focussed on Lyme disease; however, the same environmental, land use, and climatic considerations would also apply to other tick-borne pathogens.
After selection, 85 items were included for review. All literature was analyzed and synthesized by one reviewer. A complete list of search terms and the full list of results are available upon request.
Natural environments that increase the risk of tick exposures
The risk of human exposure to ticks, and potential tick-borne infections, is proportional to the amount of time an individual spends outdoors in habitats that support populations of ticks and/or their hosts. Ticks rely on host animals to survive and reproduce. While ticks are considered generalists and can feed on a broad range of species, evidence suggests that rodents, birds, and deer are common hosts for tick reproduction and movement in North America.7-10 Any environment that is suitable for such hosts can therefore be considered tick habitat.
Different habitat types differentially increase or decrease one’s risk to tick encounters. In North America, ticks are commonly found in wooded areas with leaf litter, tall grassy areas, and shrub layers as well as along forest edges, and/or within vegetated habitats under tree canopies.11-16 Wooded areas are optimal habitats for ticks as they provide a suitable microclimate (small areas with different climatic features than neighbouring areas) of leaf litter, grasses, and shrubbery, protecting ticks from weather fluctuations and extreme weather events.17 The duff layer (between the soil surface and leaf litter) in particular promotes tick survival over winter by protecting them from sub-zero temperatures.18-22 While ticks can be found in both deciduous and coniferous woodland habitats (see Text Box 1), deciduous woodlands appear to carry a greater risk of exposure to ticks due to increased leaf litter.23,24 Tree trunks and fallen logs in deciduous woodland habitats can also provide suitable habitats, especially Ixodes pacificus.25 Ticks can also exist in small patches of forested areas, including those found in residential areas; they are frequently found in leaf litter and low-growing vegetation along forest ecotones (the transition zone between forested and non-forested habitats).9,14,26 This transition between natural areas and built environments is also where people often recreate along trails.9
Other lesser-studied environments may also provide suitable habitats for ticks. For example, a recent study in California identified coastal areas with shrubs as a suitable habitat for hosts and identified ticks positive for Borrelia species.27 This highlights the bias of researching tick-borne pathogens in more traditional woodland and grassland habitats, when in reality ticks may be present in any habitat that can support the host-vector relationship.27 As the geographic range of ticks expands, it is feasible for ticks to establish themselves in new, previously unstudied habitats if the conditions are favourable. This can lead to unexpected tick exposures and highlights the need for surveillance across all landscapes.
Box 1: Deciduous versus coniferous habitats
Deciduous habitats predominantly contain trees with leaves that fall off annually. The leaves on the trees are broad and flat and change colour in autumn from green to red, orange, and yellow, and then fall off. This creates leaf litter. Examples of trees found in such habitats include maple, oak, and birch trees.28
Coniferous habitats, also known as evergreen or needle-leaved trees, predominantly contain trees with cones and needles. These trees stay green year round. Examples include cedar, pine, spruce, and fir trees.28
Built environment considerations that impact tick populations
Changing land use patterns are significant contributors to increasing zoonotic disease outbreaks worldwide.29 Changes to the natural landscape can create suitable habitats for ticks and hosts, and are linked to increased tick activity and an increase in potential human encounters with ticks and tick-borne pathogens.23,30-36 Tick density and movement are primarily impacted by changes to the built environment and forest fragmentation (change of natural continuous forests into smaller sections due to human development and urbanization).
Land use changes
While natural environments are the primary habitats for ticks, land use changes in urban, suburban, and rural areas where people live, work, and recreate are increasingly providing suitable habitats for ticks. Rapid development of housing in forested areas creates a network of forest patches (or islands) that can provide ecological connectivity to nearby natural habitats, facilitating tick movement into residential areas.7 For example, landscaped areas with canopy cover provide both a suitable habitat for animal hosts and prevent desiccation of ticks, thereby facilitating survival and movement into residential areas and urban green spaces.7 Log and brush piles in residential areas, ornamental plants, and larger properties also provide suitable habitats for ticks, thereby increasing potential tick encounters.7,26 Ticks can also travel long distances on migratory birds and be dispersed into new urban and suburban settings.23,37
In Northeastern United States where Ixodes scapularis is endemic, the risk of encountering ticks and tick-borne infections in built environments containing green spaces with abundant vegetated walkways and associated nature preserves is equivalent to the highest reported incidences from natural environments across the country.38 Yuan and colleagues (2020) found ticks positive for pathogens in school playgrounds and parks in New York State.39 Such research highlights the diverse spread of ticks in endemic areas and the need for active surveillance programs in built environments as tick encounters become more frequent in Canada.
However, not all built environments promote ticks. Some landscape features and practices such as maintaining bare soil and short grass lawns surrounding parklands have been shown to reduce tick populations.8,15,26,40,41
There is also a tension between development and promoting urban biodiversity and greenspaces while minimizing risk of exposure to ticks.42 It is clear that the built environment and landscape design have implications for tick populations in urban and suburban areas, especially with the push to increase green spaces, pollinator gardens, and movements towards rewilding. Such initiatives are important for pollinators, ecosystem services, and conservation efforts, and they support public health efforts encouraging time in nature and cardiovascular exercise.34,40,43 However, they may also increase the risk of tick encounters and potential tick-borne infections.44,45 This relationship is not well understood, and is likely non-linear and interconnected — highlighting the importance of an interdisciplinary One Health approach in examining the problem.46 At a minimum, it warrants additional research especially as municipal, provincial, and federal governments increasingly prioritize parks and other green space development such as pollinator gardens.
Land or forest fragmentation occurs through deforestation and urbanization of natural continuous forests into smaller sections.35 Historically, the transition of forests to agricultural lands and for firewood collection in Northeastern United States led to a reduction in white-tailed deer and likely restricted the movement of tick species. This was followed by human population growth and the transition of agricultural areas to suburban areas. This land use change led to the development of residential areas and a network of reforested areas, followed by an increase in white-tailed deer due to the creation of suitable habitats. In turn, tick populations increased.47,48
The addition of roads and trails through forested areas creates a patchy network of landscapes, altering vector-host ecological dynamics and spatial patterns, and facilitating host movement along new pathways.49,50 While forest fragmentation has many ecological impacts, when considering host ecology (such as deer and rodents), understanding the interaction of human and vector-host movement patterns is critical. Forest fragmentation can:
- Increase the density of deer populations. Deer populations benefit from the edge habitats created by forest fragmentation due to the absence of predators and winter foraging opportunities.51-53
- Reduce species diversity. Forest fragmentation leads to habit loss, thereby reducing species diversity. This in turn increases white-footed mice populations (a dominant host species in small forest patches and competent reservoir for tick-borne pathogens).30,51,52,54,55 Interestingly, vertebrate host biodiversity has been shown to reduce nymph infection prevalence and may offer an opportunity to reduce tick-borne pathogens by supporting biodiversity preservation efforts.55,56
- Increase potential human exposure to ticks. Forest fragmentation creates more opportunities for human engagement with forest habitats through residential properties and/or trails in edge habitats.53
While in general forest fragmentation is positively correlated to tick density and tick-infection prevalence,30,57 research also shows lower Lyme disease incidence in fragmented areas despite higher tick densities, highlighting other contextual drivers of human exposure.51 For example, small predator/prey ecological dynamics of the coyote and red fox have been shown to be a better predictor of Lyme disease in New York than deer abundance.58 Additional research is warranted to tease apart the true relationship between forest fragmentation, host diversity, and tick-borne pathogens across different contexts.51,54,57
Tick populations and climate change
The influence of changing land use priorities on the expanding range of ticks in North America is, and will increasingly be, further complicated and amplified by climate change.1,59 In the United States, the incidence of Lyme disease is expected to increase by 20% in the next 1–2 decades due to climate change.60 In Canada, ticks are predicted to expand northwards 35–55 km per year.3 Climate change is predicted to increase temperatures and change precipitation patterns, both of which could lead to extreme weather events such as floods and droughts.18,34 The exact effect of the changing conditions on tick abundance will depend on the microclimate and geography of any given habitat, and is predicted to influence tick populations both directly and indirectly (i.e., through changes in host populations). Additional research and analysis is necessary to understand how such events will impact tick population establishment and re-establishment after extreme weather events across landscapes.
Direct environmental influences
Climate-change-driven shifts that have a direct influence on tick ranges include temperature, humidity, precipitation, and more frequent extreme weather events.
Temperature: Tick life cycle and mortality are influenced by temperature. Increasing temperatures in temperate and cold environments can lead to faster maturation of nymph ticks, shorter life cycles, increased tick abundance, and longer duration of tick activity.1,34,61 Higher temperatures also increase the number of days per year and number of hours per day that ticks can seek and acquire a host.18 Sustained temperature increases can also lead to the northward expansion and establishment of non-native tick species.61-63 Conversely, rising temperatures in already arid environments can reduce tick activity and increase mortality through desiccation, and can lead to evolutionary changes.18,24,34
Species-specific responses to temperature changes are seen across tick vectors. Dermacentor species, Amblyomma americannum and Haemaphysalis longicornis ticks are more tolerant of environmental stresses and can survive in drier and hotter environments.7,11 While these tick species are currently not established in Canada, they may become endemic with sustained climate warming. Ixodes ticks are more sensitive to environmental variability and prefer higher moisture areas, such as under leaf litter or forest canopy.11 Tick species can behaviourally adapt to unfavourable environmental conditions by modifying their activity levels.18 For example, the rate of mortality among some populations of the Ixodes scapularis has increased due to desiccation. This in turn has led ticks to reduce activity in hot and dry conditions and to shelter in the duff layer, below the leaf litter, to minimize the likelihood of desiccation.18,21,64 This characteristic also protects ticks from cold temperatures, and reduces mortality, as ticks are able to seek insulated habitats (e.g., snow and duff layer) to facilitate overwintering.18,22 Such behaviour changes can either increase or decrease tick-human pathogen transmission cycles, depending on the scenario.64
Humidity: High relative humidity can increase tick survival rates at higher temperatures.65-67 This increases host-seeking activity, thereby increasing reproductive success, reducing mortality, and influencing total population density.18,21,34,68 Areas with consistent high humidity levels allow for prolonged tick activity in a given day, as compared to more arid habitats.24,68,69 Relative humidity is also highly variable based on the microclimate. This leads to spatial variability in the impact of humidity on tick populations.68
Precipitation: Increased precipitation can decrease tick activity levels and thereby slow down nymph development.1,34 However, some predictions show that precipitation can facilitate the establishment of endemic tick populations.3 Additional research is necessary to better understand the impact of total precipitation on tick populations.
Extreme weather events: Events such as flooding and droughts can decrease tick populations through direct mortality, reduction in host-seeking behaviour and/or by limiting the availability of hosts.18,19,44,70-72 Flooding can cover tick habitats with silt, while temperatures above 30 degrees Celsius can cause ticks to reduce summer activity levels, leading to increased subsequent fall and winter activity levels.44
Shifts in weather and climate warming also have the potential to increase suitable habitats across Canadian landscapes as ticks move to higher latitudes and altitudes.1,18,34,73,74 While there is some variability in how tick species and tick life stages react to climatic factors, increasing temperature is the most important predictor of tick population establishment and suitability as tick life cycle and mortality are predominantly influenced by temperature.3,18 There is limited research on the dynamic between temperature, humidity, and precipitation across tick life stages.75 For example, Ixodes scapularis will quest for hosts at lower heights in higher temperatures and low relative humidity.76 Additional research is needed to further understand the interplay between climatic factors across population and ecological processes.
Tick activity can also be indirectly influenced by climate change and resulting habitat changes, through impacts to their host species. Given that ticks rely on host species for their life cycle, the primary indirect influence is the availability and abundance of host populations, and alternation of predator-prey dynamics that may be linked to climate-change-driven habitat changes.3,18,32,77,78 For example, the white-tailed deer (a known host for tick species) has been predominately concentrated along the southern border of Canada, but is expected to increase its range 100 km further north into the Albertan boreal forest, along river corridors, over the next 50 years due climate change.77
Sustained extreme weather events (e.g., flooding) may decrease suitable tick habitats (e.g., deposit silt on tick habitats, rendering them unfavourable), decrease tick activity, and increase tick mortality via predators.18,32,77,79,80 It can also alter host population movement patterns. Such weather events may also alter land use changes and human behaviours in tick habitats (e.g., recreational activities, mushrooming, and picnics).78
The true impact of climate change is hard to determine given the many permutations of scale- and context-dependent variables that are influenced by specific microhabitats.3 Research shows that the range of tick species is expanding, but that the changes in tick density and rate of infection with pathogens are not uniform.81 Risk maps for specific tick species (Ixodes scapularis) in Canada suggest the establishment of endemic tick populations across southern parts of Canada, east of the Rocky Mountains, and northwards.82-84 This provides a helpful narrative for public health initiatives. However, favourable changes in climate and habitat suitability will only increase the likelihood of the transmission of tick-borne infections.1 As such, additional research is warranted to accurately predict the risk of ticks and tick-borne infections across Canada to better understand the spatial movement of hosts, the establishment of tick vectors across Canadian landscapes, and the complex ecological epidemiological relationship.3,78,85
Landscape changes, forest fragmentation, and climate change can increase tick populations and tick-related risks. The disease transmission cycle of tick-borne infections is part of a complex system that includes vectors, animal hosts, and humans. It is driven by many context dependent ecological and social factors. It is known that: 1) the geographic expansion of tick species into northern latitudes, and the potential of tick-borne infections, continues to pose a public health risk in Canada as ticks migrate north at a rate of 35–55 km per year in Canada; 2) climate change and land use changes (including suburban development leading to forest fragmentation and landscaped built environments) will increase suitable habitats for tick species.3 The greatest predictors of the establishment of tick populations in new geographical locations are climatic factors (particularly temperature) and the availability of host populations. Given that the tick life cycle relies on animal hosts to survive and reproduce, it is not surprising that tick geographic range is intrinsically tied to host ecology.
However, the relationships are complex and depend on a wide range of scale- and context-dependent ecological and social factors. Additional research, following an interdisciplinary or One Health approach, is warranted to tease apart the impact of climate change, land use changes, and forest fragmentation on tick density and tick infection prevalence to better understand the spatial movement of hosts, the establishment of tick vectors across Canadian landscapes, and the complex ecological and epidemiological relationship. Specifically, research gaps include: 1) the synergies between climatic factors in the expansion and survival of tick species; 2) the impact of forest fragmentation on tick populations across ecological and social contexts; 3) the role of biodiversity, conservation, and rewilding efforts in establishing suitable tick habitats.
This review also reiterates the importance of surveillance programs in non-traditional tick habitats. In the absence of climate-change mitigation, it also reinforces the need for municipal, provincial, and federal governments to consider evidence-based research, environmental health, and tick-related risks in urban policy, urban greening efforts, land use planning, and health communication. By understanding the environments and landscape features that are correlated with tick abundance, we can be better informed on how to plan and communicate public health messages to reduce the risk of tick encounters and burden of disease.
The author would like to thank NCCEH staff Dr. Leah Rosenkrantz, Dr. Anne-Marie Nicol, Dr. Lydia Ma, and Dr. Sarah Henderson for their guidance in developing this review, and Michele Wiens for literature search support. The author would also like to thank Stefan Iwasawa, Centre for Coastal Health (CCH) and BCCDC, and Dr. Colin Bates, Quest University Canada, for reviewing this paper.
- Bouchard C, Dibernardo A, Koffi JK, Wood H, Leighton P, Lindsay L. Tick-borne disease with climate and environmental changes. Can Commun Dis Rep. 2019 Apr 4;45(4). Available from: https://doi.org/10.14745/ccdr.v45i04a02.
- Gage KL, Burkot TR, Eisen RJ, Hayes EB. Climate and vectorborne diseases. Am J Prev Med. 2008 Nov;35(5):436-50. Available from: https://doi.org/10.1016/j.amepre.2008.08.030.
- Leighton PA, Koffi JK, Pelcat Y, Lindsay LR, Ogden NH. Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol. 2012 Apr;49(2):457-64. Available from: https://doi.org/10.1111/j.1365-2664.2012.02112.x.
- Randolph SE. The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B Biol Sci. 2001 Jul 29;356(1411):1045-56. Available from: https://doi.org/10.1098/rstb.2001.0893.
- Pfäffle M, Littwin N, Muders SV, Petney TN. The ecology of tick-borne diseases. Int J Parasitol. 2013 Nov;43(12-13):1059-77. Available from: https://doi.org/10.1016/j.ijpara.2013.06.009.
- Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129 Suppl:S3-14. Available from: https://doi.org/10.1017/s0031182004005967.
- Gregory N, Fernandez MP, Diuk-Wasser M. Risk of tick-borne pathogen spillover into urban yards in New York City. Parasit Vectors. 2022 Aug 10;15(1):288. Available from: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-022-05416-2.
- VanAcker MC, Little EAH, Molaei G, Bajwa WI, Diuk-Wasser MA. Enhancement of risk for lyme disease by landscape connectivity, New York, New York, USA. Emerg Infect Dis. 2019 Jun;25(6):1136-43. Available from: https://doi.org/10.3201/eid2506.181741.
- Lindsay L, Ogden N, Schofield S. Review of methods to prevent and reduce the risk of Lyme disease. Can Commun Dis Rep. 2015 Jun 4;41(6):146-53. Available from: https://doi.org/10.14745/ccdr.v41i06a04.
- McCoy KD, Léger E, Dietrich M. Host specialization in ticks and transmission of tick-borne diseases: a review. Front Cell Infect Microbiol. 2013 Oct 4;3:57. Available from: https://doi.org/10.3389/fcimb.2013.00057.
- Tick Talk. Tick facts. [cited 2022 Aug 11]; Available from: https://ticktalkcanada.com/tick-facts/.
- Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, Solomon T. Tick-borne encephalitis virus - a review of an emerging zoonosis. J Gen Virol. 2009 Aug;90:1781-94. Available from: https://doi.org/10.1099/vir.0.011437-0.
- National Collaborating Centre for Infectious Diseases. Anaplasmosis. National Collaborating Centre for Infectious Diseases. Winnipeg, MB: NCCID; 2021 [cited 2022]; Available from: https://nccid.ca/debrief/anaplasmosis/.
- Ogden NH, Lindsay LR, Schofield SW. Methods to prevent tick bites and Lyme disease. Clin Lab Med. 2015 Dec;35(4):883-99. Available from: https://doi.org/10.1016/j.cll.2015.07.003.
- Lubelczyk CB, Elias SP, Rand PW, Holman MS, Lacombe EH, Smith RP, Jr. Habitat associations of Ixodes scapularis (Acari: Ixodidae) in Maine. Environ Entomol. 2004 Aug 1;33(4):900-6. Available from: https://doi.org/10.1603/0046-225X-33.4.900.
- Stafford KC. Tick management handbook. An integrated homeowners, pest control operators, and public health officials for the prevention of tick-associated disease. New Haven, CT: Connecticut Agricultural Experiment Station; 2007. Report No.: 1010. Available from: https://stacks.cdc.gov/view/cdc/11444.
- Lindsay L, Mathison S, Barker I, Mcewen S, Gillespie T, Surgeoner G. Microclimate and habitat in relation to Ixodes scapularis (Acari : Ixodidae) populations on Long Point, Ontario, Canada. J Med Entomol. 1999 May;36(3):255-62. Available from: https://doi.org/10.1093/jmedent/36.3.255.
- Ogden N, Ben Beard C, Ginsberg H, Tsao J. Possible effects of climate change on Ixodid ticks and the pathogens they transmit: predictions and observations. J Med Entomol. 2021 Jul;58(4):1536-45. Available from: https://doi.org/10.1093/jme/tjaa220.
- Lindsay LR, Barker IK, Surgeoner GA, McEwen SA, Gillespie TJ, Robinson JT. Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. J Med Entomol. 1995 Mar 1;32(2):143-52. Available from: https://doi.org/10.1093/jmedent/32.2.143.
- Brunner JL, Killilea M, Ostfeld RS. Overwintering survival of Nymphal Ixodes scapularis (Acari: Ixodidae) under natural conditions. J Med Entomol. 2012 Sep 1;49(5):981-7. Available from: https://doi.org/10.1603/ME12060.
- Burtis JC, Sullivan P, Levi T, Oggenfuss K, Fahey TJ, Ostfeld RS. The impact of temperature and precipitation on blacklegged tick activity and Lyme disease incidence in endemic and emerging regions. Parasit Vectors. 2016 Nov 25;9(1):606. Available from: https://doi.org/10.1186/s13071-016-1894-6.
- Burtis JC, Fahey TJ, Yavitt JB. Survival and energy use of Ixodes scapularis nymphs throughout their overwintering period. Parasitology. 2019 May;146(6):781-90. Available from: https://doi.org/10.1017/s0031182018002147.
- Bouchard C, Leonard E, Koffi JK, Pelcat Y, Peregrine A, Chilton N, et al. The increasing risk of Lyme disease in Canada. Can Vet J. 2015 Jul;56(7):693-9. Available from: https://www.ncbi.nlm.nih.gov/pubmed/26130829.
- Eisen RJ, Eisen L, Girard YA, Fedorova N, Mun J, Slikas B, et al. A spatially-explicit model of acarological risk of exposure to Borrelia burgdorferi-infected Ixodes pacificus nymphs in northwestern California based on woodland type, temperature, and water vapor. Ticks Tick Borne Dis. 2010 Mar 1;1(1):35-43. Available from: https://doi.org/10.1016/j.ttbdis.2009.12.002.
- Lane RS, Mun J, Peribáñez MA, Stubbs HA. Host-seeking behavior of Ixodes pacificus (Acari: Ixodidae) nymphs in relation to environmental parameters in dense-woodland and woodland-grass habitats. J Vector Ecol. 2007 Dec;32(2):342-57. Available from: https://doi.org/10.3376/1081-1710(2007)32[342:hboipa]2.0.co;2.
- Maupin GO, Fish D, Zultowsky J, Campos EG, Piesman J. Landscape ecology of Lyme disease in a residential area of Westchester County, New York. Am J Epidemiol. 1991 Jun 1;133(11):1105-13. Available from: https://doi.org/10.1093/oxfordjournals.aje.a115823.
- Salkeld DJ, Lagana DM, Wachara J, Porter WT, Nieto NC. Examining prevalence and diversity of tick-borne pathogens in questing Ixodes Pacificus ticks in California. Appl Environ Microbiol. 2021 Jun 11;87(13):e0031921. Available from: https://doi.org/10.1128/aem.00319-21.
- Tree Canada. Trees of Canada. Ottawa, ON: Tree Canada; [cited 2022 Nov 4]; Available from: https://treecanada.ca/resources/trees-of-canada/.
- Patz JA, Graczyk TK, Geller N, Vittor AY. Effects of environmental change on emerging parasitic diseases. Int J Parasitol. 2000 Nov;30(12-13):1395-405. Available from: https://doi.org/10.1016/s0020-7519(00)00141-7.
- Allan BF, Keesing F, Ostfeld RS. Effect of forest fragmentation on Lyme disease risk. Conserv Biol. 2003;17(1):267-72. Available from: https://doi.org/10.1046/j.1523-1739.2003.01260.x.
- Public Health Agency of Canada. Lyme disease surveillance in Canada: Preliminary annual report 2019. Ottawa, ON: PHAC; 2022 Jan 28. Available from: https://www.canada.ca/en/public-health/services/publications/diseases-conditions/lyme-disease-surveillance-report-2019.html.
- Simon JA, Marrotte RR, Desrosiers N, Fiset J, Gaitan J, Gonzalez A, et al. Climate change and habitat fragmentation drive the occurrence of Borrelia burgdorferi, the agent of Lyme disease, at the northeastern limit of its distribution. Evol Appl. 2014 Aug;7(7):750-64. Available from: https://doi.org/10.1111/eva.12165.
- McClure M, Diuk-Wasser M. Reconciling the entomological hazard and disease risk in the Lyme disease system. Int J Environ Res Public Health. 2018 May 22;15(5):E1048. Available from: https://doi.org/10.3390%2Fijerph15051048.
- Ogden N, Lindsay L. Effects of climate and climate change on vectors and vector-borne diseases: ticks are different. Trends Parasitol. 2016 Aug;32(8):646-56. Available from: https://doi.org/10.1016/j.pt.2016.04.015.
- Society for Conservation Biology. Forest fragmentation may increase Lyme disease risk. ScienceDaily. 2003. Available from: https://www.sciencedaily.com/releases/2003/01/030130081414.htm.
- Roome A, Wander K, Garruto RM. Cat ownership and rural residence are associated with Lyme disease prevalence in the northeastern United States. Int J Environ Res Public Health. 2022 May 5;19(9):5618. Available from: https://doi.org/10.3390%2Fijerph19095618.
- Ogden N, Lindsay L, Hanincova K, Barker I, Bigras-Poulin M, Charron D, et al. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol. 2008 Mar;74(6):1780-90. Available from: https://doi.org/10.1128/aem.01982-07.
- Roome A, Spathis R, Hill L, Darcy JM, Garruto RM. Lyme disease transmission risk: seasonal variation in the built environment. Healthcare. 2018 Jul 19;6(3):E84. Available from: https://doi.org/10.3390%2Fhealthcare6030084.
- Yuan Q, Llanos-Soto SG, Gangloff-Kaufmann JL, Lampman JM, Frye MJ, Benedict MC, et al. Active surveillance of pathogens from ticks collected in New York State suburban parks and schoolyards. Zoonoses Public Health. 2020 Sep;67(6):684-96. Available from: https://doi.org/10.1111/zph.12749.
- Lerman SB, D'Amico V. Lawn mowing frequency in suburban areas has no detectable effect on Borrelia spp. vector Ixodes scapularis (Acari: Ixodidae). PLoS ONE. 2019 Apr 3;14(4):e0214615. Available from: https://doi.org/10.1371/journal.pone.0214615.
- Duffy DC, Clark DD, Campbell SR, Gurney S, Perello R, Simon N. Landscape patterns of abundance of Ixodes scapularis (Acari: Ixodidae) on Shelter Island, New York. J Med Entomol. 1994 Nov;31(6):875-9. Available from: https://doi.org/10.1093/jmedent/31.6.875.
- Aronson MF, Lepczyk CA, Evans KL, Goddard MA, Lerman SB, MacIvor JS, et al. Biodiversity in the city: key challenges for urban green space management. Front Ecol Environ. 2017;15(4):189-96. Available from: https://doi.org/10.1002/fee.1480.
- Lerman SB, Contosta AR, Milam J, Bang C. To mow or to mow less: lawn mowing frequency affects bee abundance and diversity in suburban yards. Biol Conserv. 2018 May 1;221:160-74. Available from: https://doi.org/10.1016/j.biocon.2018.01.025.
- van Oort BEH, Hovelsrud GK, Risvoll C, Mohr CW, Jore S. A mini-review of ixodes ticks climate sensitive infection dispersion risk in the nordic region. Int J Environ Res Public Health. 2020 Aug;17(15):5387. Available from: https://doi.org/10.3390/ijerph17155387.
- Millins C, Gilbert L, Medlock J, Hansford K, Thompson DB, Biek R. Effects of conservation management of landscapes and vertebrate communities on Lyme borreliosis risk in the United Kingdom. Philos Trans R Soc Lond B Biol Sci. 2017 Jun 5;372(1722):20160123. Available from: https://doi.org/10.1098/rstb.2016.0123.
- Stephen C. One Health: a primer for environmental public health practice [guidance document]. Vancouver, BC: National Collaborating Centre for Environmental Health; 2022 Sep 14. Available from: https://ncceh.ca/documents/guide/one-health-primer-environmental-public-health-practice.
- Eisen RJ, Eisen L. The blacklegged tick, ixodes scapularis: an increasing public health concern. Trends Parasitol. 2018 Apr;34(4):295-309. Available from: https://doi.org/10.1016/j.pt.2017.12.006.
- Spielman A. The emergence of Lyme disease and human babesiosis in a changing environment. Ann N Y Acad Sci. 1994 Dec 15;740:146-56. Available from: https://doi.org/10.1111/j.1749-6632.1994.tb19865.x.
- Talbot B, Slatculescu A, Thickstun CR, Koffi JK, Leighton PA, McKay R, et al. Landscape determinants of density of blacklegged ticks, vectors of Lyme disease, at the northern edge of their distribution in Canada. Sci Rep. 2019 Nov 13;9(1):16652. Available from: https://www.nature.com/articles/s41598-019-50858-x.
- Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, et al. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in Eastern United States. Am J Trop Med Hyg. 2012 Feb 1;86(2):320-7. Available from: https://doi.org/10.4269/ajtmh.2012.11-0395.
- Brownstein JS, Skelly DK, Holford TR, Fish D. Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia. 2005 Dec;146(3):469-75. Available from: https://doi.org/10.1007/s00442-005-0251-9.
- Barbour AG, Fish D. The biological and social phenomenon of Lyme disease. Science. 1993 Jun 11;260(5114):1610-6. Available from: https://doi.org/10.1126/science.8503006.
- Frank DH, Fish D, Moy FH. Landscape features associated with Lyme disease risk in a suburban residential environment. Landscape Ecology. 1998 Feb 1;13(1):27-36. Available from: https://link.springer.com/article/10.1023/A:1007965600166.
- Eisen RJ, Piesman J, Zielinski-Gutierrez E, Eisen L. What do we need to know about disease ecology to prevent Lyme disease in the northeastern United States? J Med Entomol. 2012 Jan;49(1):11-22. Available from: https://doi.org/10.1603/ME11138.
- LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA. 2003 Jan 21;100(2):567-71. Available from: https://doi.org/10.1073/pnas.0233733100.
- Schmidt KA, Ostfeld RS. Biodiversity and the dilution effect in disease ecology. Ecology. 2001 Mar;82(3):609-19. Available from: https://doi.org/10.1890/0012-9658(2001)082[0609:BATDEI]2.0.CO;2.
- Killilea ME, Swei A, Lane RS, Briggs CJ, Ostfeld RS. Spatial dynamics of Lyme disease: a review. Ecohealth. 2008 Jun;5(2):167-95. Available from: https://doi.org/10.1007/s10393-008-0171-3.
- Levi T, Kilpatrick AM, Mangel M, Wilmers CC. Deer, predators, and the emergence of Lyme disease. Proc Natl Acad Sci USA. 2012 Jul 3;109(27):10942-7. Available from: https://doi.org/10.1073/pnas.1204536109.
- Sonenshine DE. Range expansion of tick disease vectors in North America: implications for spread of tick-borne disease. Int J Environ Res Public Health. 2018 Mar;15(3):478. Available from: https://doi.org/10.3390/ijerph15030478.
- Dumic I, Severnini E. "Ticking bomb": the impact of climate change on the incidence of Lyme Disease. Can J Infect Dis Med Microbiol. 2018 Oct 24:5719081. Available from: https://doi.org/10.1155/2018/5719081.
- Bouchard C, Dibernardo A, Koffi J, Wood H, Leighton P, Lindsay L. N Increased risk of tick-borne diseases with climate and environmental changes. Can Commun Dis Rep. 2019 Apr 4;45(4):83-9. Available from: https://doi.org/10.14745/ccdr.v45i04a02.
- Ogden NH, Gachon P. Climate change and infectious diseases: what can we expect? Can Commun Dis Rep. 2019 Apr 4;45(4):76-80. Available from: https://doi.org/10.14745/ccdr.v45i04a01.
- Brownstein JS, Holford TR, Fish D. Effect of climate change on Lyme Disease risk in North America. Ecohealth. 2005 Mar;2(1):38-46. Available from: https://doi.org/10.1007/s10393-004-0139-x.
- Ginsberg HS, Albert M, Acevedo L, Dyer MC, Arsnoe IM, Tsao JI, et al. Environmental factors affecting survival of immature Ixodes scapularis and implications for geographical distribution of Lyme disease: the climate/behavior hypothesis. PLoS ONE. 2017 Dec 1;12(1). Available from: https://doi.org/10.1371%2Fjournal.pone.0168723.
- Beard CB, Eisen RJ, Barker CM, Garofalo JF, Hahn M, Hayden M, et al. Ch. 5: Vectorborne diseases. Washington, DC: U.S. Global Change Research Program; 2016 Apr 4. Available from: https://health2016.globalchange.gov/vectorborne-diseases.
- Schulze TL, Jordan RA. Meteorologically mediated diurnal questing of Ixodes scapularis and Amblyomma Americanum (Acari: Ixodidae) nymphs. J Med Entomol. 2003 Jul 1;40(4):395-402. Available from: https://doi.org/10.1603/0022-2585-40.4.395.
- Estrada-Peña A. Increasing habitat suitability in the United States for the tick that transmits Lyme disease: a remote sensing approach. Environ Health Perspect. 2002 Jul;110(7):635-40. Available from: https://doi.org/10.1289%2Fehp.110-1240908.
- Berger KA, Ginsberg HS, Dugas KD, Hamel LH, Mather TN. Adverse moisture events predict seasonal abundance of Lyme disease vector ticks (Ixodes scapularis). Parasit Vectors. 2014 Apr 14;7:181. Available from: https://parasitesandvectors.biomedcentral.com/articles/10.1186/1756-3305-7-181.
- Eisen RJ, Eisen L, Castro MB, Lane RS. Environmentally related variability in risk of exposure to lyme disease spirochetes in Northern California: effect of climatic conditions and habitat type. Environ Entomol. 2003 Oct 1;32(5):1010-8. Available from: https://doi.org/10.1603/0046-225X-32.5.1010.
- Bidder LA, Asmussen KM, Campbell SE, Goffigan KA, Gaff HD. Assessing the underwater survival of two tick species, Amblyomma Americanum and Amblyomma maculatum. Ticks Tick Borne Dis. 2019 Jan;10(1):18-22. Available from: https://doi.org/10.1016/j.ttbdis.2018.08.013.
- Weiler M, Duscher GG, Wetscher M, Walochnik J. Tick abundance: a one year study on the impact of flood events along the banks of the river Danube, Austria. Exp Appl Acarol. 2017 Feb;71(2):151-7. Available from: https://doi.org/10.1007%2Fs10493-017-0114-1.
- Ogden NH, Lindsay LR, Beauchamp G, Charron D, Maarouf A, O'Callaghan CJ, et al. Investigation of relationships between temperature and developmental rates of tick ixodes scapularis (Acari: Ixodidae) in the laboratory and field. J Med Entomol. 2004 Jul 1;41(4):622-33. Available from: https://doi.org/10.1603/0022-2585-41.4.622.
- Clow KM, Leighton PA, Ogden NH, Lindsay LR, Michel P, Pearl DL, et al. Northward range expansion of Ixodes scapularis evident over a short timescale in Ontario, Canada. PLoS ONE. 2017 Dec 27;12(12):e0189393. Available from: https://doi.org/10.1371/journal.pone.0189393.
- Ogden N, Bigras-Poulin M, Hanincova K, Maarouf A, O'Callaghan C, Kurtenbach K. Projected effects of climate change on tick phenology and fitness of pathogens transmitted by the North American tick Ixodes scapularis. J Theor Biol. 2008 Oct 7;254(3):621-32. Available from: https://doi.org/10.1016/j.jtbi.2008.06.020.
- Ostfeld R, Brunner J. Climate change and Ixodes tick-borne diseases of humans. Philos Trans R Soc Lond B Biol Sci. 2015 Apr 5;370(1665). Available from: https://doi.org/10.1098%2Frstb.2014.0051.
- Schulze TL, Jordan RA, Hung RW. Effects of selected meterological factors on diurnal questing of Ixodes scapularis and Amblyomma Americanum (Acari: Ixodidade). J Med Entomol. 2001 Mar;38(2):318-24. Available from: https://doi.org/10.1603/0022-2585-38.2.318.
- Dawe KL, Boutin S. Climate change is the primary driver of white-tailed deer (Odocoileus virginianus) range expansion at the northern extent of its range; land use is secondary. Ecol Evol. 2016 Sep;6(18):6435-51. Available from: https://doi.org/10.1002/ece3.2316.
- Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E. Effects of climate change on ticks and tick-borne diseases in Europe. Interdisc Perspect Infect Dis. 2009:593232. Available from: https://doi.org/10.1155/2009/593232.
- Samish M, Alekseev E. Arthropods as predators of ticks (Ixodoidea). J Med Entomol. 2001 Jan;38(1):1-11. Available from: https://doi.org/10.1603/0022-2585-38.1.1.
- MacDonald A. Abiotic and habitat drivers of tick vector abundance, diversity, phenology and human encounter risk in southern California. PLoS ONE. 2018 Jul 31;13(7). Available from: https://doi.org/10.1371/journal.pone.0201665.
- Tuite AR, Greer AL, Fisman DN. Effect of latitude on the rate of change in incidence of Lyme disease in the United States. CMAJ open. 2013 Jan;1(1):E43-7. Available from: https://doi.org/10.9778/cmajo.20120002.
- McPherson M, Garcia-Garcia A, Cuesta-Valero F, Beltrami H, Hansen-Ketchum P, MacDougall D, et al. Expansion of the Lyme disease vector Ixodes scapularis in Canada inferred from CMIP5 climate projections. Environ Health Perspect. 2017 May;125(5). Available from: https://doi.org/10.1289/EHP57.
- Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG, et al. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol. 2006 Jan;36(1):63-70. Available from: https://doi.org/10.1016/j.ijpara.2005.08.016.
- Prairie Climate Centre. Lyme disease under climate change. Winnipeg, MB: Climate Atlas of Canada; [cited 2022 Sep 29]; Available from: https://climateatlas.ca/lyme-disease-under-climate-change#:~:text=Longer%20summers%20also%20mean%20a,hosts%20that%20carry%20the%20disease.
- Ogden NH, St-Onge L, Barker IK, Brazeau S, Bigras-Poulin M, Charron DF, et al. Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr. 2008 May 22;7:24. Available from: https://doi.org/10.1186/1476-072x-7-24.
Dr. Negar Elmieh
BSc, University of Victoria; MS & MPH, Tufts University; PhD, University of British Columbia
Dr. Negar Elmieh is a Professor at Quest University in BC, Canada. She is an interdisciplinary researcher and educator and an advocate for health and environmental issues. Her interests lie at the intersection of environmental health and risk communication with a focus on emerging and re-emerging infectious diseases.