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Survival and energy use of Ixodes scapularis nymphs throughout their overwintering period

Published online by Cambridge University Press:  14 January 2019

James C. Burtis*
Affiliation:
Department of Natural Resources, Cornell University, 310 Fernow Hall, Ithaca NY 14853, USA Department of Entomology, Cornell University, 3132 Comstock Hall, Ithaca NY 14853, USA
Timothy J. Fahey
Affiliation:
Department of Natural Resources, Cornell University, 310 Fernow Hall, Ithaca NY 14853, USA
Joseph B. Yavitt
Affiliation:
Department of Natural Resources, Cornell University, 310 Fernow Hall, Ithaca NY 14853, USA
*
Author for correspondence: James C. Burtis, E-mail: jb766@cornell.edu

Abstract

The blacklegged tick (Ixodes scapularis) spends up to 10 months in the soil between feeding as larvae and questing for hosts as nymphs the following year. We tracked the survival and energy use of 4320 engorged larvae evenly divided across 288 microcosms under field conditions from September to July on sites with high (>12 nymphs/150 m2) and low (<1.2 nymphs/150 m2) densities of naturally questing I. scapularis in New York State. Subsets of microcosms were destructively sampled periodically during this period to determine tick survivorship and physiological age. Across all sites tick mortality was low during the winter and increased in the spring and early summer, coincident with increasing energy use. Neither energy use nor mortality differed significantly between sites with high vs low natural tick density, but we did observe a significant positive relationship between soil organic matter content and the survival of I. scapularis during the spring. Our results suggest that the off-host mortality and energy use of I. scapularis nymphs is relatively low in the winter and increases significantly in the spring and early summer.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

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References

Amador, JA, Wang, Y, Savin, MC and Görres, JH (2000) Fine-scale spatial variability of physical and biological soil properties in Kingston, Rhode Island. Geoderma 98, 8394.Google Scholar
Arsnoe, IM, Hickling, GJ, Ginsberg, HS, McElreath, R and Tsao, JI (2015) Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human Lyme disease risk. PLoS ONE 10, e0127450.Google Scholar
Awerbuch, TE and Sandberg, S (1995) Trends and oscillations in tick population dynamics. Journal of Theoretical Biology 175, 511516.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7.Google Scholar
Belozerov, VN (1982) Diapause and biological rhythms in ticks. In Obenchain, FD and Galun, R (eds), Physiology of Ticks. New York, NY, USA: Elsevier, pp. 469500.Google Scholar
Berg, B (2000) Litter decomposition and organic matter turnover in northern forest soils. Forest Ecology and Management 133, 1322.Google Scholar
Berger, KA, Ginsberg, HS, Dugas, KD, Hamel, LH and Mather, TN (2014) Adverse moisture events predict seasonal abundance of Lyme disease vector ticks (Ixodes scapularis). Parasites & Vectors 7, 181.Google Scholar
Bertrand, MR and Wilson, ML (1996) Microclimate-dependent survival of unfed adult Ixodes scapularis (Acari: Ixodidae) in nature: life cycle and study design implications. Journal of Medical Entomology 33, 619627.Google Scholar
Bertrand, MR and Wilson, ML (1997) Microhabitat-independent regional differences in survival of unfed Ixodes scapularis nymphs (Acari: Ixodidae) in Connecticut. Journal of Medical Entomology 34, 167172.Google Scholar
Boehnke, D, Gebhardt, R, Petney, T and Norra, S (2017) On the complexity of measuring forests microclimate and interpreting its relevance in habitat ecology: the example of Ixodes ricinus ticks. Parasites & Vectors 10, 549.Google Scholar
Brunner, JL, Killilea, M and Ostfeld, RS (2012) Overwintering survival of nymphal Ixodes scapularis (Acari: Ixodidae) under natural conditions. Journal of Medical Entomology 49, 981987.Google Scholar
Burks, CS, Stewart, RL, Needham, GR and Lee, RE (1996) The role of direct chilling injury and inoculative freezing in cold tolerance of Amblyomma americanum, Dermacentor variabilis and Ixodes scapularis. Physiological Entomology 21, 4450.Google Scholar
Burtis, JC (2017) Method for the efficient deployment and recovery of Ixodes scapularis (Acari: Ixodidae) nymphs and engorged larvae from field microcosms. Journal of Medical Entomology 54, 17781782.Google Scholar
Burtis, JC and Pflueger, C (2017) Interactions between soil-dwelling arthropod predators and Ixodes scapularis under laboratory and field conditions. Ecosphere (Washington, DC) 8, e01914.Google Scholar
Burtis, JC, Sullivan, P, Levi, T, Oggenfuss, K, Fahey, TJ and Ostfeld, RS (2016 a) The impact of temperature and precipitation on blacklegged tick activity and Lyme disease incidence in endemic and emerging regions. Parasites & Vectors 9, 606.Google Scholar
Burtis, JC, Ostfeld, RS, Yavitt, JB and Fahey, TJ (2016 b) The relationship between soil arthropods and the overwinter survival of Ixodes scapularis (Acari: Ixodidae) under manipulated snow cover. Journal of Medical Entomology 53, 225229.Google Scholar
Christenson, L, Clark, H, Livingston, L, Heffernan, E, Campbell, J, Driscoll, C, Groffman, P, Fahey, T, Fisk, M, Mitchell, M and Templer, PH (2017) Winter climate change influences on soil faunal distribution and abundance: implications for decomposition in the northern forest. Northeastern Naturalist 24, B209B234.Google Scholar
Clow, KM, Ogden, NH, Lindsay, LR, Michel, P, Pearl, DL and Jardine, CM (2017) The influence of abiotic and biotic factors on the invasion of Ixodes scapularis in Ontario, Canada. Ticks and Tick-Borne Disease 8, 554563.Google Scholar
Durden, LA and Keirans, JE (1996) Nymphs of the Genus Ixodes (Acari: Ixodidae) of the United States: Taxonomy, Identification key, Distribution, Hosts, and Medical/Veterinary Importance. Annapolis, MD, USA: Entomological Society of America.Google Scholar
Eisen, RJ, Eisen, L, Ogden, NH and Beard, CB (2016) Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and Lyme disease in North America. Journal of Medical Entomology 53, 250261.Google Scholar
Ettema, CH and Wardle, DA (2002) Spatial soil ecology. Trends in Ecology & Evolution 17, 177183.Google Scholar
Ginsberg, HS and Zhioua, E (1996) Nymphal survival and habitat distribution of Ixodes scapularis and Amblyomma americanum ticks (Acari: Ixodidae) on Fire Island, New York, USA. Experimental and Applied Acarology 20, 533544.Google Scholar
Goldin, A (1987) Reassessing the use of loss-on-ignition for estimating organic matter content in noncalcareous soils. Communications in Soil Science and Plant Analysis 18, 11111116.Google Scholar
Gray, JS, Kahl, O, Lane, RS, Levin, ML and Tsao, JI (2016) Diapause in ticks of the medically important Ixodes ricinus species complex. Ticks and Tick-Borne Diseases 7, 9921003.Google Scholar
Herrmann, C and Gern, L (2012) Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks? Parasitology 139, 330337.Google Scholar
Herrmann, C, Voordouw, MJ and Gern, L (2013) Ixodes ricinus ticks infected with the causative agent of Lyme disease, Borrelia burgdorferi sensu lato, have higher energy reserves. International Journal of Parasitology 43, 477483.Google Scholar
Holm, S (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 6570.Google Scholar
Jones, CJ and Kitron, UD (2000) Populations of Ixodes scapularis (Acari: Ixodidae) are modulated by drought at a Lyme disease focus in Illinois. Journal of Medical Entomology 37, 408415.Google Scholar
Keesing, F, Brunner, J, Duerr, S, Killilea, M, LoGiudice, K, Schmidt, K, Vuong, H and Ostfeld, RS (2009) Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society of London B: Biological Sciences 276, 39113919.Google Scholar
Killilea, ME, Swei, A, Lane, RS, Briggs, CJ and Ostfeld, RS (2008) Spatial dynamics of Lyme disease: a review. EcoHealth 5, 167195.Google Scholar
Kuznetsova, A, Brockhoff, PB and Christensen, RH (2017) Lmertest package: tests in linear mixed effects models. Journal of Statistical Software 82, 126.Google Scholar
Levi, T, Keesing, F, Oggenfuss, K and Ostfeld, RS (2015) Accelerated phenology of blacklegged ticks under climate warming. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20130556.Google Scholar
Levin, ML and Fish, D (1998) Density-dependent factors regulating feeding success of Ixodes scapularis larvae (Acari: Ixodidae). Journal of Parasitology 84, 3643.Google Scholar
Lindsay, LR, Barker, IK, Surgeoner, GA, McEwen, SA, Gillespie, TJ and Robinson, JT (1995) Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. Journal of Medical Entomology 32, 143152.Google Scholar
Lindsay, LR, Barker, IK, Surgeoner, GA, Mcewen, SA, Gillespie, TJ and Addison, EM (1998) Survival and development of the different life stages of Ixodes scapularis (Acari: Ixodidae) held within four habitats on Long Point, Ontario, Canada. Journal of Medical Entomology 35, 189199.Google Scholar
Lubelczyk, CB, Elias, SP, Rand, PW, Holman, MS, Lacombe, EH and Smith, RP Jr (2004) Habitat associations of Ixodes scapularis (Acari: Ixodidae) in Maine. Environmental Entomology 33, 900906.Google Scholar
Monaghan, AJ, Moore, SM, Sampson, KM, Beard, CB and Eisen, RJ (2015) Climate change influences on the annual onset of Lyme disease in the United States. Ticks and Tick-Borne Diseases 6, 615622.Google Scholar
Mount, GA, Haile, DG and Daniels, E (1997) Simulation of blacklegged tick (Acari: Ixodidae) population dynamics and transmission of Borrelia burgdorferi. Journal of Medical Entomology 34, 461484.Google Scholar
Nelson, CA, Saha, S, Kugeler, KJ, Delorey, MJ, Shankar, MB, Hinckley, AF and Mead, PS (2015) Incidence of clinician-diagnosed Lyme disease, United States, 2005–2010. Emerging Infectious Diseases 21, 1625–1231.Google Scholar
NOAA (2018) Land-Based Station Data. Retrieved from United State National Oceanic and Atmospheric Administration website. Available at https://www.ncdc.noaa.gov/data-access/land-based-station-data (Accessed 10 October 2017).Google Scholar
Ogden, NH and Lindsay, LR (2016) Effects of climate and climate change on vectors and vector-borne diseases: ticks are different. Trends in Parasitology 32, 646656.Google Scholar
Ogden, NH, Lindsay, LR, Beauchamp, G, Charron, D, Maarouf, A, O'callaghan, CJ, Waltner-Toews, D and Barker, IK (2004) Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. Journal of Medical Entomology 41, 622633.Google Scholar
Ogden, NH, Bigras-Poulin, M, O'callaghan, CJ, Barker, IK, Lindsay, LR, Maarouf, A, Smoyer-Tomic, KE, Waltner-Toews, D and Charron, D (2005) A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. International Journal of Parasitology 35, 375389.Google Scholar
Ogden, NH, Radojevic, M, Wu, X, Duvvuri, VR, Leighton, PA and Wu, J (2014) Estimated effects of projected climate change on the basic reproductive number of the Lyme disease vector Ixodes scapularis. Environmental Health Perspectives 122, 631.Google Scholar
Ostfeld, RS and Brunner, JL (2015) Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20140051.Google Scholar
Ostfeld, RS, Cepeda, OM, Hazler, KR and Miller, MC (1995) Ecology of Lyme disease: habitat associations of ticks (Ixodes scapularis) in a rural landscape. Ecological Applications 5, 353361.Google Scholar
Ostfeld, RS, Hazler, KR and Cepeda, OM (1996) Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape. Journal of Medical Entomology 33, 9095.Google Scholar
Ostfeld, RS, Canham, CD, Oggenfuss, K, Winchcombe, RJ and Keesing, F (2006) Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biology 4, e145.Google Scholar
Pardanani, N and Mather, TN (2004) Lack of spatial autocorrelation in fine-scale distributions of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 41, 861864.Google Scholar
Parton, WJ, Schimel, DS, Cole, CV and Ojima, DS (1987) Analysis of factors controlling soil organic matter levels in great plains grasslands1. Soil Science Society of America Journal 51, 11731179.Google Scholar
Perret, JL, Guerin, PM, Diehl, PA, Vlimant, M and Gern, L (2003) Darkness induces mobility, and saturation deficit limits questing duration, in the tick Ixodes ricinus. Journal of Experimental Biology 206, 18091815.Google Scholar
Pool, JR (2018) Lipid Use in Blacklegged Ticks (Ixodes Scapularis): Response to Aging, Infection, and Changing Weather Patterns (Ph.D. Dissertation). Fordham University, Bronx, New York, p. 144.Google Scholar
Pool, JR, Petronglo, JR, Falco, RC and Daniels, TJ (2017) Energy usage of known-age blacklegged ticks (Acari: Ixodidae): what is the best method for determining physiological age? Journal of Medical Entomology 54, 949956.Google Scholar
R Core Development Team (2017) R: A language and environment for statistical computing. Available at https://www.R-project.org/.Google Scholar
Randolph, SE and Storey, K (1999) Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741748.Google Scholar
Schulte, EE, Kaufmann, C and Peter, JB (1991) The influence of sample size and heating time on soil weight loss-on-ignition. Communications in Soil Science and Plant Analysis 22, 159168.Google Scholar
Schulze, TL, Jordan, RA and Hung, RW (1997) Biases associated with several sampling methods used to estimate abundance of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). Journal of Medical Entomology 34, 615623.Google Scholar
Steele, GM and Randolph, SE (1985) An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.)(Acari: Ixodidae). I. A unimodal seasonal activity pattern. Bulletin of Entomological Research 75, 489500.Google Scholar
USDA (2017) Web Soil Survey. Retrieved from United States Department of Agriculture website. Available at https://websoilsurvey.sc.egov.usda.gov/App/WebSoilSurvey.aspx (Accessed 10 October 2017).Google Scholar
Uspensky, I (1995) Physiological age of ixodid ticks: aspects of its determination and application. Journal of Medical Entomology 32, 751764.Google Scholar
Vail, SG and Smith, G (1998) Air temperature and relative humidity effects on behavioral activity of blacklegged tick (Acari: Ixodidae) nymphs in New Jersey. Journal of Medical Entomology 35, 10251028.Google Scholar
Van Es, RP, Hillerton, JE and Gettinby, G (1998) Lipid consumption in Ixodes ricinus (Acari: Ixodidae): temperature and potential longevity. Bulletin of Entomological Research 88, 567573.Google Scholar
Vandyk, JK, Bartholomew, DM, Rowley, WA and Platt, KB (1996) Survival of Ixodes scapularis (Acari: Ixodidae) exposed to cold. Journal of Medical Entomology 33, 610.Google Scholar
Vreeken-Buijs, MJ, Hassink, J and Brussaard, L (1998) Relationships of soil microarthropod biomass with organic matter and pore size distribution in soils under different land use. Soil Biology and Biochemistry 30, 97106.Google Scholar
Wu, X, Duvvuri, VR, Lou, Y, Ogden, NH, Pelcat, Y and Wu, J (2013) Developing a temperature-driven map of the basic reproductive number of the emerging tick vector of Lyme disease Ixodes scapularis in Canada. Journal of Theoretical Biology 319, 5061.Google Scholar
Yuval, B and Spielman, A (1990) Duration and regulation of the developmental cycle of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 196201.Google Scholar
Zhang, T (2005) Influence of the seasonal snow cover on the ground thermal regime: an overview. Reviews of Geophysics 43, 123.Google Scholar
Zuur, A, Leno, EN, Walker, N, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY, USA: Springer-Verlag.Google Scholar
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