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Changes in Abundance of the Ixodes scapularis Say (Blacklegged Tick) in Adair County, Missouri, from 2006 to 2015
Emily N. Hahn and Stephanie A. Foré

Northeastern Naturalist, Volume 26, Issue 1 (2019): 137–140

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Northeastern Naturalist Vol. 26, No. 1 E.N. Hahn and S.A. Foré 2019 137 2019 NORTHEASTERN NATURALIST 26(1):137–140 Changes in Abundance of the Ixodes scapularis Say (Blacklegged Tick) in Adair County, Missouri, from 2006 to 2015 Emily N. Hahn1 and Stephanie A. Foré1,* Abstract - Ixodes scapularis (Blacklegged Tick), vector of Lyme disease, has a broad distribution in eastern North America, but is relatively rare in Missouri. In this study, we report the change in abundance of this species in Adair County, MO, from 2006 to 2015. We collected data from 85 small-mammal trapping sessions beginning in 2006, and from 175 off-host sampling sessions using both drag and bait sampling beginning in 2007. The total number of Blacklegged Ticks collected in this study was 182; we collected less than 10 Blacklegged Ticks in most years. However, we collected 61.5% of specimens in 2014 and 86% in the last 3 years. Systematic, long-term monitoring has provided information about the dynamics of a tick species with low abundance. Introduction Ixodes scapularis Say (Blacklegged Tick), a hard tick that must take a blood meal from three different hosts to complete its life cycle, is the main vector of several pathogens of humans and other animals including Lyme disease. Recent revision of the county-scale distribution of the Blacklegged Tick in the US (Eisen et al. 2016), indicates that the number of counties that reported an established population by 2015 had more than doubled since the 1996 report (Dennis et al.1998). Eisen et al. (2016) argue that this expansion is not just an artifact of increased interest in the species, as there have been concurrent observed changes in distribution of Lyme-disease in humans. Genetic studies also provide evidence of range expansion (Khatchikian et al. 2015, Leo et al. 2017). Modeling suggests that habitat suitability is changing in the US, providing new zones for tick survival and development (Estrada-Peña 2002). Dennis et al. (1998) and Eisen et al. (2016) defined established populations as counties in which 6 or more ticks or 2 or more life stages have been found in a single collection period. In Missouri, 20% of the counties had an established population by 2015, an increase of 1.7% from 1996 (Eisen et al. 2016). This increase was due to a change in the status of 2 counties—Cape Girardeau and Adair. In Adair County, Blacklegged Ticks were not reported in a 2006 nymph survey (Diuk-Wasser et al. 2010). The objective of this study was to report the change in the number of collected Blacklegged Ticks from 2006 to 2015 in Adair County, MO. We first reported the presence of Blacklegged Ticks when 1 adult and 1 nymph were captured in 2007 as part of an on-going tick-monitoring study (Petry et al. 2010). Long-term systematic 1Department of Biology, Truman State University, Kirksville, MO 63501. *Corresponding author - sfore@truman.edu. Manuscript Editor: Christopher M. Heckscher Northeastern Naturalist 138 E.N. Hahn and S.A. Foré 2019 Vol. 26, No. 1 collection provides natural history information that will lead to an understanding of the demographic changes of this species. Field-site Description We collected ticks from 2 permanent sampling sites ~350 m apart in Adair County, Kirksville, MO. These sites were established in 2007, as described in Petry et al. (2010), and monitored through December 2015. One site was in an old field comprised mostly of non-native grasses and shrubs on the Truman State University Farm (northeast corner of site: 40.177437°N, 92.6029816°W). The other site was in an Quercus (oak)–Carya (hickory) woodlot on private property near the farm (northeast corner of site: 40.175585°N, 92.600438°W). We mapped a 120 m x 70 m grid at each site. Prior to the establishment of these permanent sampling sites, small mammals were trapped in the same locations in 2006. Methods We collected ticks using on-host and off-host sampling methods. On-host tickmonitoring data collection began on 13 June 2006. The first year was a pilot year with 3 trapping sessions in June and 1 in both August and October; each trapping session was 4 nights with 100 live traps at each site. In 2007, we began using the 120 m x 70 m grid with 104 traps at each site, and we conducted 3 night-trapping sessions every other month from February to November (6 sessions/y). In 2009, we again expanded the number of trapping months by sampling every month except December and January due to low-temperature effects on mammals (10 total trapping sessions). One exception was in 2014 when weather conditions limited sampling to 8 months. A total of 85 on-host sampling sessions occurred throughout the length of this study. We brought all animals captured back to the lab, temporarily sedated them with ether, and removed all ticks. Ticks were stored in 95% ethanol. We marked with toe clips and returned mammals to their respective points of capture. We handled all animals according to the Animal Care Guidelines of the American Society of Mammalogists (Institutional Animal Care and Use Committee protocols and Missouri Research Collection Permits approved to S.A. Foré). Off-host tick monitoring began on 22 February 2007. We sampled both sites once every other week when temperatures were above freezing, usually 10 to 11 months of the year (minimum of 20 sampling sessions per year). We conducted a total of 175 off-host sampling sessions throughout the length of this study. In each site, we collected 8 bait and 8 drag-cloth samples using a stratified sampling method to sample over the entire area as described by Petry et al. (2010). We collected bait samples by placing ~200 g of dry ice as a tick attractant in the center of each 1 m x 1 m cloth and allowing it to to sublimate for 1 h. We collected each drag sample over 30 m with a 1 m x 1 m cloth cut into 8 strips attached to a pole; all cloths were placed in individual sealed bags. We used a hand-lens and forceps to collect ticks from each cloth and stored the specimens in 95% ethanol. We identified all ticks to species (Clifford et al. 1961, Keirans and Litwak 1989), life stage (larva, nymph, or adult), and sex (if in adult life stage). We collected over Northeastern Naturalist Vol. 26, No. 1 E.N. Hahn and S.A. Foré 2019 139 5000 samples in the 10 y of this study. We made initial identifications and entered data during the year of sampling. To verify that identification and data files were accurate, we randomly selected and verified ~10% of the samples. In addition to random samples, E.N. Hahn verified all samples reported to contain the Blacklegged Tick. Results The first record of Blacklegged Tick in our study was from off-host sampling in 2007 in which we collected 1 nymph and 1 adult (Table 1). We obtained the first record of Blacklegged Tick on-host in 2009. We collected 61.5% of the total Blacklegged Ticks in 2014 and collected none in 2010. We collected a total of 182 Blacklegged Ticks by all sampling methods in both sites from February 2007 to December 2015 (Table 1), of which 54.4% were larvae, 28.6% were nymphs, and 17.0% were adults. Larvae and nymphs made up 83% of the collection, most of which we captured on-host. We collected no adult Blacklegged Ticks from small mammals captured in this study. We obtained all but 1 of the on-host specimens from Peromyscus leucopus Rafinesque (White-footed Mouse), the most commonly captured small mammal at our study sites. We collected 1 larva from Reithrodontomys megalotis (Baird) (Western Harvest Mouse) in March 2015. Discussion Data from our ongoing monitoring in Adair County, MO, indicate that the Blacklegged Tick is established based on the criteria of Dennis et al. (1998) and Eisen et al. (2016). Hudman and Sarentini (2016) reported collecting the species in locations in the county in 2014. Given the low abundance of this species in the county, the presence of the species could go undetected without systematic surveillance. The increased number of Blacklegged Ticks collected per year suggests that the population size has increased. The change in abundance may have been influenced Table 1. Total number of each life stage of Blacklegged Tick collected on small-mammal hosts and off-host in Adair County, Missouri from 2006 to 2015. na = no off-host sampling occurred in 2006. On-host Off-host Year Larvae Nymphs Larvae Nymphs Adults Yearly total 2006 0 0 na na na 0 2007 0 0 0 1 1 2 2008 0 0 0 6 0 6 2009 0 2 0 1 2 5 2010 0 0 0 0 0 0 2011 0 1 1 0 1 3 2012 1 5 0 0 3 9 2013 0 2 1 0 9 12 2014 70 16 7 8 11 112 2015 19 9 0 1 4 33 Total 90 35 9 17 31 182 Northeastern Naturalist 140 E.N. Hahn and S.A. Foré 2019 Vol. 26, No. 1 by changes in habitat, such as warmer winter temperatures and altered vegetation cover (Estrada-Peña 2002), or other factors such as host-species composition (Lo- Giudice et al. 2008). Continued surveillance is necessary to understand what factors drive the demographic changes in the Blacklegged Tick. Acknowledgments This study would not have been possible without the efforts of numerous Truman State University undergraduate research assistants. This study received partial funding support through the National Science Foundation under UBM Grants No. 0436348 and 0926737. Literature Cited Clifford, C.M., G. Anastos, and A. Elbl. 1961. The larval ixodid ticks of the eastern United States (Acarina-Ixodidae). Miscellaneous Publications of the Entomological Society of America. 2:213–237. Dennis, D.T., T.S. Nekomoto, J.C. Victor, W.S. Paul, and J. Piesman. 1998. Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. Journal of Medical Entomology 35:629–638. Diuk-Wasser, M.A., G. Vourc’h, P. Cislo, A.G. Hoen, F. Melton, S.A. Hamer, M. Rowland, R. Cortinas, G.J. Hickling, J.I. Tsao, A.G. Barbour, U. Kitron, J. Piesman, and D. Fish. 2010. Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Global Ecology and Biogeography 19:504–514. Eisen, R.J., L. Eisen, and C.B. Beard. 2016. County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. Journal of Medical Entomology 53:349–386. Estrada-Peña, A. 2002. Increasing habitat suitability in the United States for the tick that transmits Lyme disease: A remote sensing approach. Environmental Health Perspectives 11:635–640. Hudman, D.A., and N.J. Sargentini. 2016. Detection of Borrelia, Ehrlichia, and Rickettsia spp. in ticks in northeast Missouri. Ticks and Tick-Borne Diseases 7:915–921. Keirans, J.E., and T.R. Litwak. 1989. Pictorial key to the adults of hard ticks, family Ixodidae (Ixodida: Ixodoidea), East of the Mississippi River. Journal of Medical Entomology 26:435–448. Khatchikian, C.E., M. Stone, P.B. Backenson, I.N. Wang, E. Foley, S.N. Seifert, M.Z. Levy, and D. Brisson. 2015. Recent and rapid population growth and range expansion of the Lyme disease tick vector, Ixodes scapularis, in North America. Evolution 69:1678–1689. Leo, S.S.T., A. Gonzalez, and V. Millien. 2016. The genetic signature of range expansion in a disease vector: the Black-legged Tick. Journal of Heredity 108:176–183. LoGiudice, K., S.T.K. Duerr, M.J. Newhouse, K.A. Schmidt, M.E. Killilea, and R.S. Ostfeld. 2008. Impact of host-community composition on Lyme disease risk. Ecology 89:2841–2849. Petry, W.K., S.A. Foré, L.J. Fielden, and H. Kim. 2010. A quantitative comparison of two sample methods for collecting Amblyomma americanum and Dermacentor variabilis (Acari: Ixodidae) in Missouri. Experimental and Applied Acarology 52:427–438.