From a human perspective, ticks are universally regarded as loathsome critters ostensibly lacking any redeemable qualities other than malevolently participating in the balance of nature. Many outdoor workers and recreationists doubtless share this disdain for ticks: individuals who frequent rural or semi-rural environments long enough are likely to eventually find one or more of these blood-suckers crawling on their bodies or, worse yet, firmly affixed to their skin. Although the vast majority of tick species never or seldom bite people, certain species that do may deliver a dose of disease-causing viruses, bacteria, or protozoan parasites in their spit. In the United States, for example, ticks are best known for transmitting the bacteria that cause two common and well-publicized maladies: Lyme disease (LD) and Rocky Mountain spotted fever. In 2009, LD alone accounted for approximately 30,000 confirmed (an all-time high) and about 8,500 probable cases, largely in Eastern states.
Lyme disease is caused by a group of closely related, corkscrew-shaped bacteria known as spirochetes, although only one species (Borrelia burgdorferi) is known to cause clinical illness in the United States. In California, the statewide incidence of LD is quite low, with no more than about one hundred confirmed cases reported annually, mostly in northern counties. Campers, hikers, hunters, foresters, park rangers, and, yes, some gardeners, may be especially vulnerable, because they spend so much time in potentially tick-infested habitats year-round.
The lead author and members of his research team at UC Berkeley have been studying the ticks that carry bacterial disease agents in relation to the wildlife they parasitize, and the human behaviors and environmental factors that may increase the risk of encountering infected ticks. Until 2008, these studies were carried out mainly in undisturbed natural habitats, such as chaparral or dense woodlands. The shift to public gardens in the metropolitan San Francisco Bay Area was motivated by a desire to discover what kinds of human-biting ticks occur in them, their abundance in different plant communities, and what risk, if any, they may pose to gardeners.
The Regional Parks Botanic Garden (RPBG) in Tilden Regional Park and the University of California Botanical Garden (UCBG) are located in the Berkeley Hills. Both gardens abut natural areas populated by native wildlife, including Columbian black-tailed deer, a key host for adult populations of a few species of human-biting ticks. Many wildlife species reside within the gardens, but deer have been excluded by fencing.
The RPBG comprises approximately ten acres subdivided into sections that conserve and display the diverse native plants of this ecologically diverse state. One section, presenting plants indigenous to the Berkeley Hills and fittingly dubbed the Canyon Section, consists mainly of a coast live oak (Quercus agrifolia)/ California bay (Umbellularia californica) woodland, with coastal sage scrub dominated by California sagebrush (Artemisia californica), sticky monkey flower (Diplacus aurantiacus), and California honeysuckle (Lonicera hispidula). The Canyon Section was the only area surveyed for ticks at the RPBG, because anecdotal reports indicated that most gardeners bitten by ticks probably had been parasitized there. Wildcat Creek meanders through the garden creating humid conditions favorable for the survival and development of some tick species.
The UCBG collection is global in breadth, but emphasizes plants originating in mediterranean climes. Tick sampling was confined to the California, Mediterranean, Mexico/Central America, and South America areas because they accounted for most of the tick-exposures reported previously by staff members.
All ticks have four life stages: the egg and three blood-sucking stages (larva, nymph, and adult). Protein assimilated from their meal of blood is used to complete development from larva to nymph or nymph to adult and, in the case of females, to produce a few hundred to several thousand eggs.
Many tick species have been recorded in California, but only three of them attach to people with any regularity in the greater San Francisco Bay Area: western black-legged tick (Ixodes pacificus), American dog tick (Dermacentor variabilis), and Pacific Coast tick (D. occidentalis). Of these, the aggressive, indiscriminately feeding, and widespread western blacklegged tick is the most notorious and destructive to human health, and the only one capable of transmitting the bacterium that causes LD. In Northern California, nymphs are most active from March until July, and the adult ticks from around late November until April. Larvae and nymphs imbibe blood from lizards, birds, or small mammals for several days; adult ticks feed on deer or medium-sized mammals for about a week. Only the adult females and the tiny nymphs (about the size of a poppy seed) transmit spirochetes to people.
In both gardens, adult ticks were collected in a series of transects, by dragging or flagging vegetation bordering the uphill and downhill margins of public trails with a square piece of white flannel attached to a wooden handle. All transects were sampled eight times biweekly from December 2008 to March 2009. The Canyon Section transect at the RPBG and two off-trail, leaf-litter areas at the UCBG were also dragged for nymphal ticks six times from April to June 2009. At the UCBG, one leaf-litter transect was located in the Mediterranean area next to the deer-proof fence, and the other in an undeveloped oak-woodland canyon situated due west of the California area.
The drags or flags were inspected at regular intervals for ticks, and all ticks found were preserved in ethanol for later identification and testing. Ticks were tested individually for Borrelia burgdorferi DNA and albuterol HFA with a highly sensitive molecular assay that amplifies any targeted DNA present.
To determine the abundance of western blacklegged tick larvae and nymphs in the vicinity of the adult tick transect-lines, western fence lizards (Sceloporus occidentalis) were captured live and examined for ticks. All attached ticks found were removed with fine-tipped forceps and preserved in ethanol; each lizard was released at its capture site. Western fence lizard (often called “bluebelly”) is one of the commonest lizards in the Far West. It acquires numerous host-seeking tick larvae and nymphs with vacuum cleaner-like efficiency while basking, foraging for insects and spiders, or engaging in male courtship behavioral displays that resemble push-ups.
Gardeners were asked to complete a questionnaire documenting any tick exposures they recalled in the preceding year (July 1, 2007 to June 30, 2008). For the next two years, they were asked to submit any attached or unattached ticks they found on themselves for identification and testing for Borrelia burgdorferi DNA.
Western black-legged ticks were prevalent in both gardens. Adults were obtained from all trailside transects at UCBG, except for the Oak Knoll. The highest prevalence of ticks was found in the Mediterranean area, where the abundance was about two, thirteen, and thirty-six times greater than it was in the South America, Mexico/Central America, and California main pathway areas, respectively. These wide-ranging tick densities are similar to those recorded from diverse chaparral, dense woodlands, and grasslands in Northern California. The Mediterranean area at UCBG is the only one that abuts native Northern coastal scrub dominated by coyote brush (Baccharis pilularis var. consanguinea) just outside the garden’s perimeter and through which deer trails are prevalent. Thus, the nearby presence of a natural, tick-permissive habitat and deer may contribute to the higher numbers of ticks within the Mediterranean area.
The 2009 UCBG Western fence lizard capture data were analyzed to assess the relative abundance of lizards and their associated tick burdens. Lizards were as abundant in the tick-depauperate California area as in the tick-plentiful Mediterranean area, yet nearly three times more larvae and ten times more nymphs, on average, parasitized lizards in the Mediterranean area. We concluded that lizard-population sizes, by themselves, do not determine the abundance of host-seeking larvae or adults in a given habitat.
Vegetation bordering the uphill (versus downhill) margins of trails produced the lion’s share of adult ticks. In the areas yielding the highest tick populations, approximately ninety percent of the adult ticks were gathered from uphill borders and only ten percent from downhill margins. Small differences in ambient temperature and relative humidity between vegetation bordering both sides of a trail were deemed insufficient, by themselves, to account for the marked disparity in tick abundance.
Unlike adult ticks, which quiescently lie in wait for hours or days atop low-lying vegetative perches for prospective hosts (including humans) to contact them, the more desiccation-susceptible nymphs seek their hosts in more humid groundlitter areas, or on branches, litter, logs, and trunks in moisture-laden woodlands. The abundance of nymphs in the RPBG Canyon Section and UCBG Mediterranean area was similar, whereas the abundance of nymphs in the adult tick-impoverished California undeveloped area was minuscule, as anticipated. Gardeners working in plant beds having such densities are at low risk of encountering the nymphs, as evidenced by the fact that only one unattached nymph was discovered on a gardener during the entire study period.
Those Lymey Ticks
Having established that western blacklegged ticks flourish in certain areas of both gardens, we next sought to determine if any adult or nymphal ticks were infected with LDgroup spirochetes. Most populations of this tick species investigated in northwestern California have, so far, harbored LD spirochetes, so it was not totally unexpected when some spirochete-infected ticks surfaced in both gardens. Overall, 5.4% of 130 nymphs and 3.1% of 324 adult ticks were infected at the RPBG, as were 5.4% of 37 nymphs and 0.8% of 243 adults from the UCBG Mediterranean area. Likewise, 18.2% of 11 nymphs from the undeveloped woodland adjacent to the California area and 1.8% of 113 adults from the South America area contained spirochetes. These infection levels mirror those detected in nymphs and adults collected in rural environments of northwestern California.
Tick Encounters and Risk
For the casual visitor who abides by garden rules to shun the beds and who stays to the center of the trails, the risk of contact with any disease-carrying ticks is virtually nil. Though everyone should be aware of the possibility of contracting LD from a tick bite when gardening or hiking on narrow trails (it only takes one unlucky encounter), the posting of warning signs along the wide paths of these public gardens would raise undue alarm.
For staff gardeners, the initial questionnaire revealed that they recalled few or no ticks attached to themselves within the developed or undeveloped portions of the gardens in the year prior to the study. They recalled, on average, one tick per person per year in each garden. During the two years of the study, the average number of self-reported tick bites declined by sixty percent in both gardens. These reductions may reflect random processes due to the small sample sizes, to an actual decline in local tick populations as the study progressed, or, more likely, to an increased vigilance by gardeners as a result of their active participation in the study.
By comparison, residents of a rural community at high-risk for LD in northwestern California who had been diagnosed as probably having the disease, recalled an average of close to two tick bites per year over a two-year period. In that study, subjects reportedly spent an average of twenty-six hours per week outdoors pursuing leisure or work-related activities. In our study, full-time gardeners were exposed to potentially tick-infested habitats for up to forty hours per week. These findings underscore the lower risk of tick encounters experienced by public gardeners in the Berkeley Hills, except for the individual tending the Mediterranean area at UCBG.
Western black-legged ticks submitted by garden staff were also tested for LD-group spirochetes. None of five adults from the RPBG were infected with spirochetes, but two of forty-nine ticks from the UCBG contained spirochetes. An infected male tick from the Mediterranean area was unattached at the time of discovery. The other infected tick, an adult female presumably acquired in the South Africa area, had been attached for less than eight hours; not surprisingly, that gardener did not contract LD because infected ticks usually must be attached for two or more days before spirochetes are injected via salivary secretions into the bite-wound.
Together, our findings demonstrate that LD transmission cycles are entrenched in both gardens, but the overall risk of exposure to an infected tick is quite low for gardeners and practically non-existent for the public. What little risk there is to gardeners varies strikingly according to floral type. Indeed, 35 of 49 ticks obtained from staff at the UCBG infested the gardener assigned to the Mediterranean area; this individual was bitten only once. On the other hand, 6 of the remaining 14 ticks that infested UCBG gardeners in other floral areas had attached to them. Since the other floral areas supported far fewer ticks, an inverse association may exist between tick abundance and tick-bites: the more ticks present, the lower the proportion of tick bites because of heightened awareness. This hypothesis merits further exploration, and has implications for developing and implementing public educational campaigns against ticks and tick-borne diseases.
The first line of defense against ticks has always been to utilize various personal protective measures, such as wearing protective clothing, inspecting oneself during and after visiting tick habitats, applying repellents to clothing or skin, and avoiding or minimizing risky behaviors. Spray-can formulations containing 0.5% permethrin as the active ingredient are remarkably effective for personal protection when applied to clothing. Recently, the effectiveness of four commonly used personal preventive measures for protection against LD was evaluated in Connecticut. The measures included the use of tick repellents on the skin or clothing; spraying the property with acaricides (tick pesticides); use of protective clothing (long pants, long-sleeved shirts, light-colored clothing); and checking the body for ticks. The use of protective clothing and the routine use of tick repellents were found to be the most effective in preventing LD. Hence, we recommend that gardeners working where ticks abound seriously consider wearing a pair of white overalls treated periodically with a tick repellent containing permethrin. Light-colored clothing provides a sharply contrasting background against which ticks can be discerned readily.
We realize that not all public gardens contain populations of human-biting ticks and the majority in urban areas may be tick-free. Our study was limited to two public gardens juxtaposed to natural areas where ticks and their typical wildlife hosts co-exist, and some spillover of these animals into (and out of) the gardens might be expected. Whether or not the presence of natural areas adjoining public gardens is a sine qua non for ticks to occur in them must await future surveys in different geographic regions.
The authors gratefully acknowledge the invaluable participation of the RPBG and UCBG gardeners and other staff members who contributed variously to the conduct of this research. Steve Edwards from RPBG and Paul Licht and Chris Carmichael at UCBG, whose encouragement and steadfast support made possible this study, offered helpful suggestions on an earlier version of the manuscript. We also thank Holly Forbes, Joyce E Kleinjan, Kevin Koy, Alexandria Lee-Goldman, Esther Omi-Olsen and Daniel J Salkeld for their technical assistance.
A Brief Bibliography
Lane, Robert S. 2008. “Lyme disease in California.” Pest Notes, Publication 7485. University of California Agriculture and Natural Resources.
Vásquez, Marietta, Catherine Muehlenbein, Matthew Cartter, Edward B Hayes, Starr Ertel, and Eugene D Shapiro. 2008. “Effectiveness of personal protective measures to prevent Lyme disease.” Emerging Infectious Diseases 14: 210-216.