Balsam fir needles killed overwintering ticks. The essential oils extracted from these needles were also acaricidal. The main essential oil within balsam fir, β-pinene, killed ticks too, although less effectively than the whole balsam fir essential oil. Balsam fir needles required several weeks to kill ticks, while the essential oil killed ticks in days at cold temperatures Room temperature (i.e. 20oC) reduced the tick-killing effectiveness of the essential oil (Fig. 4). Lower temperatures may have decreased the loss of the volatile compounds responsible for the tick-killing. By decreasing the loss of these compounds, the duration of the tick’s exposure to the essential oils could have been increased.
Low temperatures may aid in killing ticks for reasons other than reducing the loss of volatile substances. Low temperatures slow enzyme activity11 and could reduce the rate of detoxification, allowing toxic compounds to accumulate. In addition, detoxification pathways may be compromised by a shift in resources towards overwintering survival. In some insects, detoxification is impaired during the activation of other physiological systems (e.g. immune responses) due to competition for limited resources28. Exposure to toxic compounds may force an over-investment in detoxification; such an over-investment may impair overwintering survival29. Some insects experience oxidative stress during exposure to low temperatures30. If ticks do the same, then low temperatures could compound the toxic effects of balsam fir. Additionally, the decline in mobility at low temperatures31,32 may limit the ability of Ixodes ticks to move away from toxic leaf litter. Although this was not a serious issue in this study, as ticks were confined to tubes, it would reduce the ability of ticks to exit toxic leaf litter in the field. Even though ticks are capable of some movement in the winter32, forcing ticks to expend energy in locomotion during the winter to avoid toxic leaf litter could reduce overwintering survival during this non-feeding state. Not only will ticks be forced to consume scarce reserves, they will be more vulnerable to predation, freezing and desiccation while searching for a new patch of leaf litter. In addition, ticks exposed to balsam fir needles showed evidence of toxicity even after a short exposure (i.e. a slower righting reflex). These sublethal effects could produce a reduction in motor abilities, leaving ticks unable to find hosts. Thus, even if ticks are able to leave balsam fir leaf litter, shorter exposures may nonetheless impact tick populations.
In addition to β-pinene, other components are likely to play a role in the acaricidal effect of balsam fir essential oil. Combining essential oils can enhance their efficacy33, and balsam fir contains a number of essential oils (Table 1). Two of the main essential oils found in our locally collected balsam fir needles, α-pinene and β-pinene (Table 1), are known to be lethal to some insects34. β-pinene has also been reported to repel Amblyomma americanum and Rhipicephalus appendiculatus ticks, although it has not previously been identified as an acaricide33. In fact, α- and β-pinene were not effective at killing I. scapularis nymphs at any concentration in a previous study35 that examined their acaricidal effect at 21oC and for 24 h. α-pinene and β-pinene may be lethal only at colder temperatures. The standard method for testing whether plant compounds kill ticks is to incubate them for 15 days at 27oC36, which could explain why some low-toxicity compounds may be overlooked.
Balsam fir essential oil showed a significant repellent effect at room temperature, but it required a relatively high concentration (8% v/v) in the horizontal assay test. The repellency effect is significantly reduced after only 10 minutes, indicating the high volatility of the essential oil (Figure 3). Other plant essential oils can repel ticks (I. ricinus) at lower concentrations (e.g. lavender oil, < 1% w/w37). These results demonstrate the low persistence of balsam fir essential oil at room temperature.
These results suggest that balsam fir needles, and their essential oil, have development potential as an acaricide. Balsam fir essential oil has minimal toxicity to terrestrial vertebrates at the concentrations used in this study. (https://www.praannaturals.com/downloads/msds/SDS_Organic_Essential_Oil_Fir_Balsam_Canada.pdf). A balsam fir-derived product could provide environmentally-friendly control, especially when used during the winter when ticks are most sensitive to it. Moreover, winter application of an acaricide could offer additional ecological advantages. By late fall fewer non-target organisms are likely to be exposed38. Therefore, later applications should reduce negative impacts on pollinators39. Late application would also reduce the phytotoxicity that can occur with some essential oils39. However, the compounds in plants that are deadly to ticks probably evolved to defend plants against insect herbivores, not blood-sucking arthropods3. They have effects on ticks because of similarities in the physiology of insects and ticks3. Therefore, any development of balsam fir, or other natural product targeting the over-wintering period, should examine its effects on arthropods that over-winter in the ground, especially on soil organisms that help control ticks40.
Whether other plants can decrease tick overwintering survival should also be explored. In previous studies that showed high overwintering success in I. scapularis, the leaf litter was from deciduous trees10,18,41. Ticks appear to have better survival and are more abundant in deciduous forests during their active period (i.e., spring, summer and fall) than in coniferous forests42–45, although not all studies find these trends13,46. Nevertheless, our results suggest that some species of conifers may be a potential source of anti-tick compounds. We hypothesize it will be plants like balsam fir, with which I. scapularis ticks historically have had little experience. For example, few I. scapularis ticks are found under eastern hemlock (Tsuga canadensis L., Carrière)44, suggesting another possible northern conifer with acaricidal properties.
Although low humidity can be lethal to I. scapularis47,48, it is unlikely that the decline in tick survival in balsam fir leaf litter was because it was a poor insulator. Lindsay et al.49 found little difference in temperature or vapour pressure deficit between white pine and maple forest leaf litter over the winter. Brunner10 found no differences in the overwintering survival of I. scapularis nymphs between two sites that differed in relative humidity by about 20% (one site had 40% RH, the other had 20% RH). This result suggests that the small differences we observed in humidity between the two leaf litters in this study is unlikely to explain the very large difference in mortality.
Many people become infected with Lyme disease in their own yard; a safe, efficient acaricide could play an important role in reducing the exposure to tick bites and to the spread of these infections4. Even if a vaccine for Lyme disease becomes available, I. scapularis can vector other diseases50, and tick control will be necessary to prevent them. Our results show that a single application of balsam fir needles, or a balsam fir-based product, could be sufficient to kill overwintering ticks. Despite winter rain and periodic snow melts, a single patch of balsam fir needles was able to kill ticks in our open tube field tests. Other studies have noted that applications of acaricides prior to re-activation of ticks in the spring can significantly reduce the numbers of early season ticks7, suggesting that reducing overwintering survival will also reduce numbers in the spring51. For example, Rand et al.52 found that a low toxicity acaricide (IC2™, made with rosemary essential oil) sprayed in October substantially reduced the number of I. scapularis ticks in the following spring. However, a different study applied the same low toxicity control agent (IC2™) in June and found that it had little lasting effect6. Possibly the application of IC2™ under cold weather conditions (i.e. late October in Maine, US) enhanced its efficacy52. Cold temperatures may be an important ally of low toxicity, natural control products.