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Potential Effects of Environmental Conditions on Prairie Dog Flea Development and Implications for Sylvatic Plague Epizootics

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Abstract

Fleas are common ectoparasites of vertebrates worldwide and vectors of many pathogens causing disease, such as sylvatic plague in prairie dog colonies. Development of fleas is regulated by environmental conditions, especially temperature and relative humidity. Development rates are typically slower at low temperatures and faster at high temperatures, which are bounded by lower and upper thresholds where development is reduced. Prairie dogs and their associated fleas (mostly Oropsylla spp) live in burrows that moderate outside environmental conditions, remaining cooler in summer and warmer in winter. We found burrow microclimates were characterized by stable daily temperatures and high relative humidity, with temperatures increasing from spring through summer. We previously showed temperature increases corresponded with increasing off-host flea abundance. To evaluate how changes in temperature could affect future prairie dog flea development and abundance, we used development rates of O. montana (a species related to prairie dog fleas), determined how prairie dog burrow microclimates are affected by ambient weather, and combined these results to develop a predictive model. Our model predicts burrow temperatures and flea development rates will increase during the twenty-first century, potentially leading to higher flea abundance and an increased probability of plague epizootics if Y. pestis is present.

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References

  • Altermatt F (2010) Climatic warming increases voltinism in European butterflies and moths. Proceedings of the Royal Society B 277:1281–1287

    Article  PubMed  Google Scholar 

  • Andrewartha HG, Birch L (1986) The ecological web: More on the distribution and abundance of animals. Chicago: University of Chicago Press

    Google Scholar 

  • Araújo FR, Silva MP, Lopes AA, Ribeiro OC, Pires PP, Carvalho CME, Balbuena CB, Villas AA, Ramos JKM (1998) Severe cat flea infestation of dairy calves in Brazil. Veterinary Parasitology 80:83–86

    Article  PubMed  Google Scholar 

  • Azad A (2002) Epidemiology of murine typhus. Annual Review of Entomology 35:553–569

    Article  Google Scholar 

  • Bennett NC, Jarvis JUM, Davies KC (1988) Daily and seasonal temperatures in the burrows of African rodent moles. South African Journal of Zoology 3:189–195

    Article  Google Scholar 

  • Bevins SN, Chandler JC, Barrett N, Schmit BS, Wiscomb GW, Shriner SA (2021) Plague exposure in mammalian wildlife across the western United States. Vector Borne Zoonotic Disease 9:667–674

    Article  Google Scholar 

  • Biggins DE, Godbey JL, Gage KL, Carter LG, Montenieri JA (2010) Vector control improves survival of three species of prairie dogs (Cynomys) in areas considered enzootic for plague. Vector-Borne Zoonotic Diseases 10:17–26

    Article  PubMed  Google Scholar 

  • Biggins DE, Eads DA (2019) Prairie dogs, persistent plague, flocking fleas, and pernicious positive feedback. Frontiers in Veterinary Science 6:1–12

    Article  Google Scholar 

  • Bond R, Riddle A, Mottram L, Beugnet F, Stevenson R (2007) Survey of flea infestation in dogs and cats in the United Kingdom during 2005. Veterinary Record 160:503–506

    Article  CAS  PubMed  Google Scholar 

  • Bulova SJ (2002) How temperature, humidity, and burrow selection affect evaporative water loss in desert tortoises. Journal of Thermal Biology 27:175–189

    Article  Google Scholar 

  • Burroughs AL (1947) Sylvatic plague studies. The vector efficiency of nine species of fleas compared with Xenopsylla cheopis. Epidemiology and Infection 45:371–396

    CAS  Google Scholar 

  • Chomel BB, Kasten RW, Floyd-Hawkins K, Chi B, Yamamoto K, Roberts-Wilson J, Gurfield AN, Abbott RC, Pedersen NC, Koehler JE (1996) Experimental transmission of Bartonella henselae by the cat flea. Journal of Clinical Microbiology 34:1952–1956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damos P, Savopoulou-Soultani M (2012) Temperature-driven models for insect development and vital thermal requirements. Psyche 2012:1–13

    Article  Google Scholar 

  • Daszak P, Cunningham CC, Hyatt AD (2000) Emerging infectious disease of wildlife – threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Dunfey-Ball KR (2009) Moose density, habitat, and winter tick epizootics in a changing climate. Thesis: University of New Hampshire, Durham, New Hampshire

    Google Scholar 

  • Eads DA, Biggins DE (2015) Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America. Conservation Biology 29:1086–1093

    Article  PubMed  Google Scholar 

  • Eads DA, Abbott RC, Biggins DE, Rocke TE (2020) Flea parasitism and host survival in a plague-relevant system: theoretical and conservation implications. Journal of Wildlife Diseases 56:378–387

    Article  PubMed  Google Scholar 

  • Eisen RJ, Gage KL (2012) Transmission of flea-borne zoonotic agents. Annual Review of Entomology 57:61–82

    Article  CAS  PubMed  Google Scholar 

  • Eskey CR, Haas VH (1940) Plague in the western part of the United States. Public Health Bulletin 254:1–83

    Google Scholar 

  • Fitch HS (1948) Ecology of the California ground squirrel on grazing lands. The American Midland Naturalist 39:513–596

    Article  Google Scholar 

  • Furness RW, Furness EN (2018) Ixodes ricinus parasitism of birds increases at higher winter temperatures. Journal of Vector Ecology 43:59–62

    Article  PubMed  Google Scholar 

  • Gilbert N, Raworth DA (1996) Insects and temperature - a general theory. The Canadian Entomologist 128:1–13

    Article  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 297:2158–2162

    Article  Google Scholar 

  • Hall LS, Myers K (1978) Variations in the microclimate in rabbit warrens in semi-arid New South Wales. Australian Journal of Ecology 3:187–194

    Article  Google Scholar 

  • Holmes CJ, Dobrotka CJ, Farrow DW, Rosendale AJ, Benoit JB, Pekins PJ, Yoder JA (2018) Low and high thermal tolerance characteristics for unfed larvae of the winter tick Dermacentor albipictus (Acari: Ixodidae) with special reference to moose. Ticks and Tick-Borne Diseases 9:25–30

    Article  PubMed  Google Scholar 

  • Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. Chicago: University of Chicago Press

    Google Scholar 

  • Hubbard C (1968) Fleas of Western North America. New York: Hafner Publishing Company

    Google Scholar 

  • Hubbart JA (2011) An inexpensive alternative solar radiation shield for ambient air temperature micro-sensors. Journal of Natural & Environmental Sciences 2:9–14

    Google Scholar 

  • IPCC (2014) Climate change 2014: Synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. R.K. Pachauri and L.A. Meyer editors. Intergovernmental Panel on Climate Change, Geneva, Switzerland.

  • Kay FR, Whitford WG (1978) The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in southcentral New Mexico. American Midland Naturalist 99:270

    Article  Google Scholar 

  • Kotliar N, Miller B, Reading R, Clark T (2006) The prairie dog as a keystone species. In: Hoogland J (ed) Conservation of the Black-Tailed Prairie Dog: Saving North America’s Western Grasslands Washington, D.C.: Island Press, pp 53–64

    Google Scholar 

  • Krasnov B (2008) Functional and evolutionary ecology of fleas: A model for ecological parasitology. Cambridge: Cambridge University Press

    Book  Google Scholar 

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001a) Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38:629–637

    Article  CAS  PubMed  Google Scholar 

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001b) Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Medical and Veterinary Entomology 15:249–258

    Article  CAS  PubMed  Google Scholar 

  • Kreppel KS, Telfer S, Rajerison SM, Morse A, Baylis M (2016) Effect of temperature and relative humidity on the development times and survival of Synopsyllus fonquerniei and Xenopsylla cheopis, the flea vectors of plague in Madagascar. Parasites & Vectors 9:1–10

    Article  Google Scholar 

  • Kunkel KE, Stevens LE, Stevens SE, Sun L, Janssen E, Wuebbles D, Kruk MC, Thomas DP, Shulski MD, Umphlett NA, Hubbard KG, Robbins K, Romolo L, Akyuz A, Pathak TB, Bergantino TR, Dobson JG (2013a) Regional climate trends and scenarios for the U.S. national climate assessment. Part 4. Climate of the U.S. Great Plains. NOAA Technical Report NESDIS 142–4. NOAA National Environmental Satellite, Data, and Information Service, Washington, D.C., USA.

  • Kunkel KE, Stevens LE, Stevens SE, Sun L, Janssen E, Wuebbles D, Redmond KT, Dobson JG (2013b) Regional climate trends and scenarios for the U.S. national climate assessment. Part 5. Climate of the southwest U.S. NOAA Technical Report NESDIS 142–4. NOAA National Environmental Satellite, Data, and Information Service, Washington, D.C., USA.

  • LaPointe DA, Atkinson CT, Samuel MD (2012) Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249:211–226

    Article  PubMed  Google Scholar 

  • Liao W, Atkinson CT, LaPointe DA, Samuel MD (2017) Mitigating future avian malaria threats to Hawaiian forest birds from climate change. PLOS ONE 12:e0168880

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis RE (2002) A review of the North American species of Oropsylla Wagner and Ioff, 1926 (Siphonaptera: Ceratophyllidae: Ceratophyllinae). Journal of Vector Ecology 27:184–206

    PubMed  Google Scholar 

  • Longanecker DS, Burroughs A (1952) Sylvatic plague studies, IX. Studies of the microclimate of the California ground squirrel burrow and its relation to seasonal changes in the flea population. Ecology 33:488–499

    Article  Google Scholar 

  • Mawdsley JR, O’Malley R, Ojima DS (2009) A review of climate-change adaption strategies for wildlife management and biodiversity conservation. Conservation Biology 23:1080–1089

    Article  PubMed  Google Scholar 

  • Metzger ME (2000) Studies on the bionomics of California ground squirrel fleas and evaluation of insecticides applied topically to their hosts for control. PhD. dissertation. University of California Riverside, Riverside, CA, USA.

  • Metzger ME, Rust MK (1997) Effect of temperature on cat flea (Siphonaptera:Pulicidae) development and overwintering. Journal of Medical Entomology 34:173–178

    Article  CAS  PubMed  Google Scholar 

  • Miller B, Ceballos G, Reading R (1994) The prairie dog and biotic diversity. Conservation Biology 8:677–681

    Article  Google Scholar 

  • Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL (1999) ncidence of plague associated with increased winter-spring precipitation in New Mexico. American Journal of Tropical Medicine and Hygiene 61:814–821

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C, Ryrholm N, Stefanescu NC, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583

    Article  CAS  Google Scholar 

  • Pauli JN, Buskirk SW, Williams ES, Edwards WH (2006) A plague epizootic in the black-tailed prairie dog (Cynomys ludovicianus). Journal of Wildlife Diseases 42:74–80

    Article  PubMed  Google Scholar 

  • Pike DA, Mitchell CJ (2013) Burrow-dwelling ecosystem engineers provide thermal refugia throughout the landscape. Animal Conservation 16:694–703

    Article  Google Scholar 

  • Poje JE, Rocke TE, Samuel MD (2020) Impacts of environmental conditions on fleas in black-tailed prairie dog burrows. Journal of Vector Ecology 45:356–365

    Article  PubMed  Google Scholar 

  • Poje JE, Rocke TE, Samuel MD (2022) Temperatures of black-tailed prairie dog burrows through the U.S. Great Plains. U.S. Geological Survey data release, https://doi.org/10.5066/P93TCY21.

  • Reichman O, Smith S (1990) Burrows and burrowing behavior by mammals. Current Mammology 2:197–244

    Google Scholar 

  • Richgels KLD, Russell RE, Bron GM, Rocke TE (2016) Evaluation of Yersinia pestis transmission pathways for sylvatic plague in prairie dog populations in the western U.S. EcoHealth 13:415–427

    Article  PubMed  Google Scholar 

  • Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integrative Zoology 5:132–142

    Article  PubMed  Google Scholar 

  • Rothschild M (1965) Myxomatosis and the rabbit flea. Nature 207:1162–1163

    Article  CAS  PubMed  Google Scholar 

  • Russell RE, Abbott RC, Tripp DW, Rocke TE (2018) Local factors associated with on-host flea distributions on prairie dog colonies. Ecology and Evolution 8:8951–8972

    Article  PubMed  PubMed Central  Google Scholar 

  • Russell RE, Walsh DP, Samuel MD, Grunnill MD, Rocke TE (2021) Space matters: host spatial structure and the dynamics of plague transmission. Ecological Modelling. https://doi.org/10.1016/j.ecolmodel.2021.109450

    Article  Google Scholar 

  • Salkeld DJ, Stapp P (2008) Prevalence and abundance of fleas in black-tailed prairie dog burrows: implications for the transmission of plague (Yersinia pestis). Journal of Parasitology 94:616–621

    Article  PubMed  Google Scholar 

  • SAS Institute Inc. (2013) SAS/ACCESS® 9.4 Interface to ADABAS: Reference. Cary, NC: SAS Institute Inc.

  • Scheidt VJ (1988) Flea allergy dermatitis. Veterinary Clinics of North America: Small Animal Practice 18:1023–1042

    Article  CAS  Google Scholar 

  • Schmidt-Nielsen K (1964) Desert Animals: Physiological Problems of Heat and Water. New York: Oxford University Press

    Google Scholar 

  • Sheets RG, Linder RL, Dahlgren RB (1971) Burrow systems of prairie dogs in South Dakota. Journal of Mammalogy 52:451–453

    Article  Google Scholar 

  • Shenbrot G, Krasnov B, Khokhlova I, Demidova T, Fielden L (2002) Habitat-dependent differences in architecture and microclimate of the burrows of Sundevall’s jird (Meriones crassus) (Rodentia: Gerbillinae) in the Negev Desert, Israel. Journal of Arid Environments 51:265–279

    Article  Google Scholar 

  • Silverman J, Rust MK, Reierson DA (1981) Influence of temperature and humidity on survival and development of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Journal of Medical Entomology 18:35–78

    Article  Google Scholar 

  • Stapp P (1998) A reevaluation of the role of prairie dogs in great plains grasslands. Conservation Biology 12:1253–1259

    Article  Google Scholar 

  • Stapp P, Antolin MF, Ball M (2004) Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Niño events. Pages 235–240 in Frontiers in Ecology and the Environment, Ecological Society of America.

  • Tripp DW, Gage KL, Montenieri JA, Antolin MF (2009) Flea abundance on black-tailed prairie dogs (Cynomys ludovicianus) increases during plague epizootics. Vector-Borne and Zoonotic Diseases 9:313–321

    Article  PubMed  Google Scholar 

  • Tripp DW, Rocke TE, Runge JP, Abbott RC, Miller MW (2017) Burrow dusting or oral vaccination prevents plague-associated prairie dog colony collapse. Ecohealth 14:451–462

    Article  PubMed  PubMed Central  Google Scholar 

  • USFWS (2013) Recovery plan for the black-footed ferret (Mustela nigripes). U.S. Fish and Wildlife Service Region 6, Denver, CO, USA. 157 pp. http://www.fws.gov/endangered/species/recovery-plans.html

  • Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Tripp DW, Brinkerhoff RJ, Gage KL, Antolin MF (2008) Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. Ecohealth 205–12. doi: https://doi.org/10.1007/s10393-008-0165-1. Epub 2008 Mar 25. PMID: 18787922.

  • Williams ES, Mills K, Kwiatkowski DR, Thorne ET, Boerger-Fields A (1994) Plague in a Black-footed Ferret (Mustela nigripes). Journal of Wildlife Diseases 30:581–585

    Article  CAS  PubMed  Google Scholar 

  • Williams SK, Schotthoefer AM, Montenieri JA, Holmes JL, Vetter SM, Gage KL, Bearden SW (2013) Effects of low-temperature flea maintenance on the transmission of Yersinia pestis by Oropsylla montana. Vector Borne Zoonotic Diseases 13:468–748

    Article  PubMed  Google Scholar 

  • Wilson LT, Barnett WW (1983) Degree-days: an aid in crop and pest management. California Agriculture 37:4–7

    Google Scholar 

  • Yeruham I, Rosen S, Hadani A (1989) Mortality in calves, lambs and kids caused by severe infestation with the cat flea Ctenocephalides felis felis (Bouché, 1835) in Israel. Veterinary Parasitology 30:351–356

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the United States Department of Defense Strategic Environment Research and Development Program Number 16 RC01-012. S. Eyob, C. Malave, N. Vlotho, and G. Corriveau assisted with flea collections in the field, and N. Vlotho and G. Corrievau helped identify fleas in the laboratory. We would like to thank R. Matchett, C. Jones, P. Dobesh, T. Willman, S. Grassel, B. McCann, H. Hicks, D. Baggao, and R. Howard for their help with site selection and access. Three anonymous reviewers provided valuable comments that improved the paper. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Data are available online at https://doi.org/10.5066/P93TCY21 (Poje et al. 2022).

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Samuel, M.D., Poje, J.E., Rocke, T.E. et al. Potential Effects of Environmental Conditions on Prairie Dog Flea Development and Implications for Sylvatic Plague Epizootics. EcoHealth 19, 365–377 (2022). https://doi.org/10.1007/s10393-022-01615-6

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