Plant Invasions Increase Tick Abundance and Risk of Tick-Borne Disease in Humans

Erin Brennan

Western Kentucky University

BIOL 516 Research - Plant Ecology

22 April 2022

Introduction

Invasive species are a rapidly growing problem in the United States, causing a wide range of issues, from biodiversity loss and extinction to changes in ecosystem functions and ecosystem services to increasing rates of human disease. The problem of biological invasion has grown significantly with new biological invasions increasing by orders of magnitude in the last 200 years due to the expansion of human migration around the world and the increase in global commerce (Mack et al. 2000; Lockwood et al. 2013). The number of species that have been moved out of their native range and into a new location is growing as are the problems caused by these invaders are growing in tandem (Lockwood et al. 2013). Vast areas of terrestrial, aquatic, and marine ecosystems have been overcome by invaders making invasive species one of the most important environmental impacts of colonization, human transportation, and global commerce (Mooney & Cleland 2001). The widespread effects of human-caused biological invasions threaten efforts to conserve and protect biodiversity, and support natural ecosystems (Mack et al. 2000). However, the spread of invasive species is not simply an environmental problem. Biological invasions also pose a significant threat to human health.

Invasive plants are plants that have been introduced by humans into a novel environment in which they did not evolve and where very few factors which limit their growth and reproduction exist (Westbrooks 1998). Once established, invasive plants often cause serious ecological harm and incur significant economic costs (Westbrooks 1998; Ranney & Ranney 2004). Some invasive plants even impact human health, either directly, such as through poisoning, or indirectly, by providing habitat for or attracting hosts for organisms that carry diseases afflicting humans, such as ticks.

Invasive plants have the potential to dramatically alter habitat by spreading rapidly, out-competing native plants, and even altering the physical environment leading to major ecological changes. Oftentimes, these ecosystem changes provide habitat and attract hosts for arthropod vectors of disease. Because of these changes to ecosystems, invasive plants can create ideal conditions for arthropod vectors of disease, such as ticks and mosquitos, either due to the habitat the invasive plant provides for these organisms or the habitat it creates for their hosts (Gardner et al. 2015). In some cases, invasive plants act as attractants for or repellants against arthropod vectors of disease, impacting the populations of these organisms and changing community dynamics involving the spread of disease in an ecosystem. Invasive plants alter the structure and function of ecosystems, modifying habitat quality, which may affect the abundance and distribution of arthropod disease vectors (Lubelczyk et al. 2004; Gardner et al. 2015).

The replacement of native understory plant species with certain invasive shrubs may increase populations of arthropod vectors of disease with potentially negative consequences for human health (Gardner et al. 2015; Wei et al. 2020). There is a significant connection between vectorborne diseases and the issues surrounding invasive species. The introduction of invasive plants can significantly impact the risk of vector-borne disease. (Léger et al. 2013). The expansion of an area affected by a specific disease is often facilitated by the movement of vector species, host or reservoir species, and invasive plant species from invaded areas into uninvaded areas (Invasive Species Advisory Committee 2019). Invasive plant species play a significant role in enhancing tick, host, and tick-borne pathogen distribution and survival (Civitello et al. 2008a). Not only do invasive plants alter habitat, but they are difficult to eradicate, and create hotspots for emerging infectious diseases (Wei et al. 2020).

In this paper, I will review the wide variety of diseases impacting humans, including those spread by ticks, and the most common species of ticks that are responsible for the spread of tick-borne disease in the United States. I will then examine the impact of plant invasions on tick abundance and the risk of tick-borne disease in humans.

Vector-borne Disease

Since the start of the 20th century, the number of infectious diseases in humans has been increasing. Approximately 335 infectious diseases have emerged in humans since 1940 (Institute of Medicine et al. 2011). Approximately 60 percent of emerging diseases are zoonotic, with 72 percent being transmitted from wildlife and the rest transmitted from domestic animals, and approximately 30 percent of emerging infectious diseases are vector-borne (Institute of Medicine et al. 2011). There are currently at least 520 viruses associated with arthropods and as many as 100 of these infect humans (Mullen & Durden 2009). Arboviruses (a contraction of “arthropod-borne virus”) include over 70 types, subtypes, and varieties of viruses spread by arthropods worldwide, some of which are associated with mosquitos and some ticks (Mullen & Durden 2009). Diseases spread by ticks include bacterial infections, viruses, parasites, and a syndrome that causes allergic reactions (Mullen & Durden 2009; CDC 2016).

According to the Centers for Disease Control and Prevention, tick-borne diseases are on the rise in the United States (CDC 2016). There are many serious tick-borne diseases, but perhaps the most well-known is Lyme disease. There are more than 30,000 cases of Lyme disease reported each year in the United State, but the actual number is thought to be as high as 300,000 due to Lyme disease being extremely underreported (Institute of Medicine et al. 2011; CDC 2016). The region in which Lyme disease occurs is expanding every year. The increase in tick-borne disease outbreaks is due to climate change affecting disease vectors and the habitat of vectors and hosts (CDC 2016). The various species of ticks which carry diseases are expanding their ranges. There is also an expansion in the populations and ranges of wildlife species that serve as reservoirs and hosts for diseases, changes in land-use patterns, and other factors (CDC 2016).

Ticks in the United States

Ticks are the number two vector of disease in the world and the number one vector of disease in the United States, responsible for 95% of cases of vector-borne disease in the United States (Sonenshine 2018; Mullen & Durden 2009). Worldwide, ticks are the most important veterinary vector and second only to mosquitos in their importance to human public health (Mullen & Durden 2009; CDC 2016). Ticks transmit a greater variety of infectious organisms than any other group of blood-sucking arthropods (Mullen & Durden 2009). They transmit many protozoa, viral, bacterial, rickettsial, and fungal pathogens (Mullen & Durden 2009; CDC 2016). Ticks cause tens of thousands of cases of tick-borne disease in humans annually (Mullen & Durden 2009; CDC 2016). The bites of ticks can also cause toxic reactions, allergic responses, and even fatal paralysis (Mullen & Durden 2009).

While other species of tick bite humans, the three most common ticks in the United States that serve as vectors of disease are the Blacklegged tick, the Lone star tick, and the American dog tick. All three of these ticks spread various bacteria, protozoa, and viruses that can cause serious illness in humans (CDC 2016; Centers for Disease Control and Prevention 2019). Ixodes include the black-legged tick in the Eastern US and the western black-legged tick in the Pacific coast states. Ixodes ticks contribute to Anaplasma, Lyme disease, Ehrlichia, Babesia, Powassan virus, Tularemia, and Carrión's disease (CDC 2016). Amblyomma includes the Lone star tick and spreads Spotted Fever Group rickettsioses, Ehrlichia, Heartland virus, Bourbon virus, and Alpha gal syndrome (CDC 2016). Dermacentor includes the American dog tick and spreads Colorado Tick Fever, Spotted Fever Group, Tularemia, and Babesiosis (CDC 2016).

Figure 1. Disease-transmitting ticks in the United States: (a) Blacklegged tick (Ixodes scapularis), (b) Lone star tick (Amblyomma americanum), (c) American dog tick (Dermacentor variabilis)

Asian Longhorned Tick - A New Invasive Tick in the United States

The Asian longhorned tick (Haemaphysalis longicornis) is a newly identified invasive species first reported in the United States in 2017, however, archived specimens indicate a potential arrival date of 2010 (Egizi et al. 2020; Centers for Disease Control and Prevention 2021). The Asian longhorned tick is native to China, Japan, Korea, and southeast Russia (Egizi et al. 2020). By September 2021, Asian longhorned ticks had already spread to 17 states including Arkansas, Connecticut, Delaware, Georgia, Kentucky, Maryland, Missouri, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Rhode Island, South Carolina, Tennessee, Virginia, and West Virginia (Centers for Disease Control and Prevention 2021). Female ticks can lay eggs and reproduce without mating, which may help to explain its rapid spread, making the invasive Asian longhorned tick a species of concern (Centers for Disease Control and Prevention 2021). These ticks have been found on pets, livestock, wildlife, and humans. Compared with native ticks, the Asian longhorned tick appears to be less attracted to humans but bites from these ticks have spread serious illnesses to people and animals in other countries (Centers for Disease Control and Prevention 2021). In Asia, the longhorn tick is the primary vector of Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV), a hemorrhagic fever with high mortality rates in humans, and also transmits Rickettsia japonica, which causes Japanese spotted fever, a potentially fatal zoonotic disease (Egizi et al. 2020). Other tick-borne pathogens found in Asian longhorned ticks include Anaplasma, Borrelia, and Ehrlichia (Egizi et al. 2020).

Invasive Plants and Ticks

Invasive plant species play a significant role and likely enhance tick, host, and tick-borne pathogen survival and distribution. Non-native plants often invade areas of high human activity, such as along trails, roads, and forest edges - the same habitat favored by ticks, tick hosts, and the pathogens they carry. This convergence suggests that habitat modifications caused by plant invasions may mediate disease vector habitat quality, indirectly impacting human disease risk (Civitello et al. 2008a)

Ecosystem changes, including those caused by invasive plants, may create habitats favorable to ticks and increase the risk of exposure to tick-borne disease (Lubelczyk et al. 2004). For example, Wei et al. found that the abundance of ticks infected with bacteria that cause spotted fever found on primary hosts was much higher in sites invaded by non-native plants than in uninvaded sites (Wei et al. 2020). Elias et al. found twice as many adult ticks and almost twice as many nymphs in areas dominated by non-native invasive plants than in uninvaded areas dominated by native shrubs (Elias et al. 2006). Not only do invasive plants alter habitat, but they support ticks and their host species which are often reservoirs for disease (Wei et al. 2020).

Many invasive species contribute to the spread of tick-borne diseases. These include not only invasive tick species, species of tick native which have expanded their range, invasive disease hosts (wildlife species that serve as reservoirs of disease), invasive diseases including the bacterial, viral, or protozoal pathogens which cause tick-borne diseases, but also invasive plant species that provide ticks and hosts with beneficial habitat (Lubelczyk et al. 2004; Elias et al. 2006; Invasive Species Advisory Committee 2019; Wei et al. 2020).

Figure 7. Invasive plants that contribute to ticks and tick-borne disease: (a) Amur honeysuckle (Lonicera maackii), (b) Japanese barberry (Berberis thunbergii), (c) Eastern red cedar (Juniperus virginiana)

Honeysuckle and Blacklegged Ticks, Lone Star Ticks

Amur honeysuckle (Lonicera maackii), a species of invasive bush honeysuckle native to Asia, supports both blacklegged tick and lone star tick populations (Lubelczyk et al. 2004). Forest understories are often subjected to invasions by non-native plants such as honeysuckle which provides suitable microclimate conditions for ticks along with protective cover and abundant fruit for wildlife (Lubelczyk et al. 2004).

Honeysuckle forms dense thickets creating shelter and protection utilized by deer. White-tailed deer (Odocoileus virgin-ianus) is the major host for adult lone star ticks and a pathogen reservoir. White-tailed deer use areas with invasive honeysuckle more often than nearby areas without this plant invader. This preference leads to higher numbers of pathogen-infected ticks in honeysuckle-invaded areas than in adjacent uninvaded areas (Allan et al. 2010). Amur honeysuckle invasions increase the risk of exposure to ehrlichiosis, an emerging infectious disease transmitted by the lone star tick (Allan et al. 2010). The attraction of white-tailed deer to invasive honeysuckle and the subsequent significant increase in infected ticks in invaded areas indicates that the introduction of invasive plants can lead to an indirect increase in disease risk (Léger et al. 2013).

Areas that were cleared of invasive honeysuckle were visited less frequently by white-tailed deer and had lower densities of lone star tick nymphs, a reduction that is due to reduced use by deer rather than changes to the habitat (Allan et al. 2010). Tick-borne disease risk is reduced when invasive honeysuckle is eradicated, suggesting that management of biological invasions may lower the impacts of vector-borne diseases on human health (Allan et al. 2010).

Japanese Barberry and Blacklegged Ticks

Studies conducted by the University of Connecticut show that Japanese barberry (Berberis thunbergii) creates an ideal habitat for blacklegged ticks that need shade and humidity to survive. Japanese barberry enhances the abundance of blacklegged ticks (Lubelczyk et al. 2004). While Japanese barberry invasions have been proven to enhance tick, host, and Lyme disease pathogen densities, invasion control significantly reduces tick populations and infection prevalence (Lubelczyk et al. 2004).

In eastern forests with an overabundance of white-tailed deer, Japanese barberry has become the dominant understory shrub, which may provide a habitat favorable to blacklegged tick and white-footed mouse survival (Williams et al. 2009). Mice are a host for the black-legged tick, which transmits Lyme disease from mice to humans (Williams et al. 2009).

Adult tick populations in dense barberry were higher than in areas with controlled barberry and areas with no barberry. Further, in areas where barberry was controlled, infection prevalence was reduced (Ward et al. 2009). These results indicate that managing Japanese barberry will have a positive effect on public health by reducing the number of B. burgdorferi infected blacklegged ticks that could spread the bacteria that cause Lyme disease to humans (Ward et al. 2009).

Eastern Red Cedar and Lone Star Ticks

Eastern red cedar (Juniperus virginiana) is native to the East coast of the United States (University of Nebraska n.d.). After being planted outside of its native range for forestry and landscaping purposes, Eastern red cedar has escaped cultivation and is invading grasslands and mixed woodlands as it spreads west through the Great Plains (University of Nebraska n.d.). The lone star tick has also expanded its range and spread into these areas along with the Eastern red cedar (Noden & Dubie 2017).

Areas invaded by Eastern red cedar tend to have lower populations of birds and rodents and higher populations of deer compared to uninvaded native grasslands and mixed woodlands (Noden & Dubie 2017). This change in host species prevalence makes Eastern red cedar invaded areas less hospitable to other tick species that require rodents and other small animals for blood meals as nymphs (Noden & Dubie 2017). However, Lone star ticks are flexible feeders. All stages of lone star ticks will feed on any blood source, meaning that lone star ticks can feed on deer at any life stage (Noden & Dubie 2017). This flexibility allows it to more easily spread and invade new habitats, including those invaded by Eastern red cedar.

As forest habitats tend to have higher tick abundance than grasslands, the spread of Eastern red cedar into grasslands and the subsequent succession from grassland to forest will lead to a greater prevalence of ticks and increased risk of tick-borne disease (Rynkiewicz & Clay 2014; Noden & Dubie 2017). Lone star ticks are vectors for diseases that infect humans including spotted fever group (SFG), anaplasmosis, ehrlichiosis, and other emerging pathogens, along with AlphaGal Syndrome (CDC 2016; Centers for Disease Control and Prevention 2019). The spread of Lone star ticks in Eastern red cedar invaded areas has led to the spread of these tick-borne diseases into new states (Noden & Dubie 2017).

Japanese Stiltgrass - A Plant Invader that Decreases Tick Population

Not all invasive understory plants lead to increases in tick populations. In general, highly invasive plants tend to create habitat that supports both ticks and their host species, but Japanese stiltgrass seems to be an exception. Japanese stiltgrass (Microstegium) is highly invasive, forming dense thickets and altering habitat by out-competing native plants (Cornell University Cooperative Extension 2019).

Areas invaded by stiltgrass have lower humidity, making them inhospitable to ticks that require humidity and shade to survive (Civitello et al. 2008b). Areas invaded by Japanese stiltgrass were found to have a 13.8 percent increase in temperature and an 18.8 percent decrease in humidity when compared to nearby uninvaded areas, resulting in conditions that led to a 173 percent increase in Lone star tick mortality and a 70 percent increase in American dog tick mortality (Civitello et al. 2008b). Areas invaded by Japanese stiltgrass were found to have lower densities of ticks and therefore reduced risk of human disease (Civitello et al. 2008b). Tick populations in Japanese stiltgrass were lower than those in native vegetation, translating to a lower risk of disease in stiltgrass invaded areas.

Climate Change Impacts

Climate change is contributing to an ongoing range expansion of ticks and tick-borne pathogens, along with expanding ranges and growing populations of wildlife that serve as hosts for disease-causing pathogens. Additional factors that contribute to increases in tick-borne disease include the fragmentation of habitat, changes in land-use patterns, and increasing populations of white-tailed deer and other tick-host populations (Rynkiewicz & Clay 2014; Invasive Species Advisory Committee 2019). These factors combine to impact populations of disease vectors, hosts, and pathogens in complex ways.

Anthropogenic climate change is increasingly affecting species and ecosystems, including invasive plants, range-expanding ticks, and host species. It is important to take into consideration the ecological and human health impacts of range-shifting species (Wallingford et al. 2020). As the Earth’s climate continues to change, range shifts will be considered crucial to the survival of many species. However, some range-shifting species will alter community structure and ecosystem processes, and some, such as ticks, will escalate human health risks (Wallingford et al. 2020).

Ticks have been expanding their geological ranges and populations have increased their abundance in recent decades due to climate change, increasing severe public health threats for humans (Rynkiewicz & Clay 2014; Sonenshine 2018). Ticks have been expanding their ranges not only north but westward as well into areas that were previously unsuitable due to lack of humidity, linking these expansions to plant invasions which make the habitat more suitable for ticks and their hosts, as is occurring with invasions of Eastern red cedar and Lone star ticks (Sonenshine 2018; Noden & Dubie 2017). Tick range expansion is host-dependent and even a small number of ticks may be sufficient to establish a population if its hosts expand their range into a new area (Sonenshine 2018). The negative impacts of invasions and range expansions will continue to intensify due to the increased opportunities for invasions provided by climate change (Mazza et al. 2014).

Discussion

Once established, invasive plants cause serious ecological harm, incur economic costs, and even impact human health by providing habitat for or attracting hosts for organisms that carry diseases afflicting humans, such as ticks (Westbrooks 1998; Ranney & Ranney 2004; Lubelczyk et al. 2004). The impact of invasive plants is expected to continue to increase with anthropogenic climate change (Bradley et al. 2010; Turbelin & Catford 2021). Climate change will create more favorable conditions for invasive plants, native and invasive ticks, and hosts to expand into new ranges (Bradley et al. 2010; Wallingford et al. 2020). The ranges of many tick species are changing and expanding due to climate change and human alteration of landscapes (Rynkiewicz & Clay 2014). In addition to the impacts of climate change, habitat fragmentation, urbanization, and the expansion of agriculture are increasingly affecting species and ecosystems, including invasive plants, range-expanding ticks, and host species. Humans are putting more pressure on ecosystems than ever before, leaving us increasingly vulnerable to vector-borne and zoonotic diseases (Mazza et al. 2014).

Current research has shown that while plant invasions can lead to an increase in tick and host abundance, an increase in the risk of disease, and the spread of disease, controlling invasions of particular non-native plant species can have a positive impact on public health by limiting the risk of tick-borne disease (Allan et al. 2010; Noden & Dubie 2017; Ward et al. 2009). Additional research into the impacts of biological invasions on the spread of diseases infecting humans will be needed as the climate continues to change, as we continue to alter wild areas and come into contact with wildlife, and as our system of global commerce continues to introduce new invasive species into novel environments.

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1. Disease-transmitting ticks in the United States: (a) Blacklegged tick (Ixodes scapularis), (b) Lone star tick (Amblyomma americanum), (c) American dog tick (Dermacentor variabilis)

1. Blacklegged tick (Ixodes scapularis)

Blacklegged tick. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/tickbornediseases/tickID.html (Accessed April 2022).

2. Lone star tick (Amblyomma americanum)

Lone star tick. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/tickbornediseases/tickID.html (Accessed April 2022).

3. American dog tick (Dermacentor variabilis)

American dog tick. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/tickbornediseases/tickID.html (Accessed April 2022).

2. Figure 2. Blacklegged Tick (Ixodes scapularis) geographic distribution.

Map of Blacklegged Tick (Ixodes scapularis) Geographic Distribution. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/geographic_distribution.html (Accessed April 2022).

3. Figure 3. Western Blacklegged Tick (Ixodes pacificus) geographic distribution.

Map of Western Blacklegged Tick (Ixodes pacificus) Geographic Distribution. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/geographic_distribution.html (Accessed April 2022).

4. Figure 4. Lone Star Tick (Amblyomma americanum) geographic distribution.

Map of Lone Star Tick (Amblyomma americanum) Geographic Distribution. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/geographic_distribution.html (Accessed April 2022).

5. Figure 5. American Dog Tick (Dermacentor variabilis) geographic distribution.

Map of American Dog Tick (Dermacentor variabilis) Geographic Distribution. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/geographic_distribution.html (Accessed April 2022).

6. Figure 6. Asian longhorned tick (Haemaphysalis longicornis)

Asian longhorn tick. Centers for Disease Control and Prevention. Available from https://www.cdc.gov/ticks/longhorned-tick/index.html (Accessed April 2022).

7. Figure 7. Invasive plants that contribute to ticks and tick-borne disease: (a) Amur honeysuckle (Lonicera maackii), (b) Japanese barberry (Berberis thunbergii), (c) Eastern red cedar (Juniperus virginiana)

1. Amur honeysuckle (Lonicera maackii)

Mehrhoff L. Image Number 5272075. University of Connecticut. Available from https://www.forestryimages.org/browse/detail.cfm?imgnum=5272075 (Accessed April 2022).

2. Japanese barberry (Berberis thunbergii)

Mehrhoff L. Image Number 5456971. University of Connecticut. Available from https://www.forestryimages.org/browse/detail.cfm?imgnum=5456971 (Accessed April 2022).

3. Eastern red cedar (Juniperus virginiana)

Schwartz H. Image Number 5366071. Colorado State University. Available from https://www.forestryimages.org/browse/detail.cfm?imgnum=5366071 (Accessed April 2022).