• 1.

    Nava S 2018. Rhipicephalus sanguineus (Latreille, 1806): neotype designation, morphological re-description of all parasitic stages and molecular characterization. Ticks Tick-borne Dis 9: 15731585.

    • Search Google Scholar
    • Export Citation
  • 2.

    Zemtsova GE, Apanaskevich DA, Reeves WK, Hahn M, Snellgrove A, Levin ML, 2016. Phylogeography of Rhipicephalus sanguineus sensu lato and its relationships with climatic factors. Exp Appl Acarol 69: 191203.

    • Search Google Scholar
    • Export Citation
  • 3.

    Murphy GL, Ewing SA, Whitworth LC, Fox JC, Kocan AA, 1998. A molecular and serologic survey of Ehrlichia canis, E. chaffeensis, and E. ewingii in dogs and ticks from Oklahoma. Vet Parasitol 79: 325339.

    • Search Google Scholar
    • Export Citation
  • 4.

    Stoffel RT 2014. Experimental infection of Rhipicephalus sanguineus with Ehrlichia chaffeensis. Vet Microbiol 172: 334338.

  • 5.

    Rovery C, Brouqui P, Raoult D, 2008. Questions on Mediterranean spotted fever a century after its discovery. Emerg Infect Dis 14: 13601367.

  • 6.

    Demma LJ 2005. Rocky Mountain spotted fever from an unexpected tick vector in Arizona. N Engl J Med 353: 587594.

  • 7.

    Parola P, Socolovschi C, Jeanjean L, Bitam I, Fournier PE, Sotto A, Labauge P, Raoult D, 2008. Warmer weather linked to tick attack and emergence of severe rickettsioses. PLoS Negl Trop Dis 2: e338.

    • Search Google Scholar
    • Export Citation
  • 8.

    Álvarez-Hernández G, Roldán JFG, Milan NSH, Lash RR, Behravesh CB, Paddock CD, 2017. Rocky Mountain spotted fever in Mexico: past, present, and future. Lancet Infect Dis 17: e189e196.

    • Search Google Scholar
    • Export Citation
  • 9.

    Eremeeva ME 2011. Rickettsia rickettsii in Rhipicephalus ticks, Mexicali, Mexico. J Med Entomol 48: 418421.

  • 10.

    Villarreal Z, Stephenson N, Foley J, 2018. Possible northward introgression of a tropical lineage of Rhipicephalus sanguineus ticks at a site of emerging Rocky Mountain spotted fever. J Parasitol 104: 240245.

    • Search Google Scholar
    • Export Citation
  • 11.

    Dantas-Torres F, Figueredo LA, Brandão-Filho SP, 2006. Rhipicephalus sanguineus (Acari: ixodidae), the brown dog tick, parasitizing humans in Brazil. Rev Soc Bras Med Trop 39: 6467.

    • Search Google Scholar
    • Export Citation
  • 12.

    Goddard J, 1989. Focus of human parasitism by the brown dog tick, Rhipicephalus sanguineus (Acari: ixodidae). J Med Entomol 26: 628631.

    • Search Google Scholar
    • Export Citation
  • 13.

    Walker J, Keirans J, Horak I, 2000. The Genus Rhipicephalus (Acari, Ixodidae): A Guide to the Brown Ticks of the World .Cambridge, England: Cambridge University Press.

    • Search Google Scholar
    • Export Citation
  • 14.

    Rhodes AR, Norment BR, 1979. Hosts of Rhipicephalus sanguineus (Acari: ixodidae) in northern Mississippi, USA. J Med Entomol 16: 488492.

  • 15.

    Martins TF, Reis JL, Viana EB, Luz HR, Oda FH, Dantas SP, Labruna MB, 2020. Ticks (Acari: ixodidae) on captive and free-ranging wild animals in Tocantins state, a cerrado-amazon transition region of northern Brazil. Int J Acarol 46: 254257.

    • Search Google Scholar
    • Export Citation
  • 16.

    Jones EO, Gruntmeir JM, Hamer SA, Little SE, 2017. Temperate and tropical lineages of brown dog ticks in North America. Vet Parasitol Reg Stud Rep 7: 5861.

    • Search Google Scholar
    • Export Citation
  • 17.

    Labruna MB, Gerardi M, Krawczak FS, Moraes-Filho J, 2017. Comparative biology of the tropical and temperate species of Rhipicephalus sanguineus sensu lato (Acari: ixodidae) under different laboratory conditions. Ticks Tick-borne Dis 8: 146156.

    • Search Google Scholar
    • Export Citation
  • 18.

    Schaefer C, Allen J, Yao T, Owen H, Lisowski S, VandenBrooks J, 2019. The phylogenetics of Rhipicephalus sanguineus and its role as a vector of Rocky Mountain spotted fever. FASEB J 33: lb296.

    • Search Google Scholar
    • Export Citation
  • 19.

    Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, Diuk-Wasser MA, 2012. Vector host-feeding preferences drive transmission of multi-host pathogens: west Nile virus as a model system. Proc R Soc B Biol Sci 279: 925933.

    • Search Google Scholar
    • Export Citation
  • 20.

    Spengler JR, Estrada-Peña A, 2018. Host preferences support the prominent role of Hyalomma ticks in the ecology of Crimean-Congo hemorrhagic fever. PLoS Negl Trop Dis 12: e0006248.

    • Search Google Scholar
    • Export Citation
  • 21.

    Randolph SE 2008. Variable spikes in tick-borne encephalitis incidence in 2006 independent of variable tick abundance but related to weather. Parasit Vectors 1: 44.

    • Search Google Scholar
    • Export Citation
  • 22.

    Haggart DA, Davis EE, 1980. Ammonia-sensitive neurones on the first tarsi of the tick, Rhipicephalus sanguineus. J Insect Physiol 26: 517523.

    • Search Google Scholar
    • Export Citation
  • 23.

    Estrada-Peña A, Jongejan F, 1999. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23: 685715.

    • Search Google Scholar
    • Export Citation
  • 24.

    Socolovschi C, Raoult D, Parola P, 2009. Influence of temperature on the attachment of Rhipicephalus sanguineus ticks on rabbits. Clin Microbiol Infect 15: 326327.

    • Search Google Scholar
    • Export Citation
  • 25.

    Carroll JF, 1999. Notes on responses of blacklegged ticks (Acari: ixodidae) to host urine. J Med Entomol 36: 212215.

  • 26.

    Uspensky I, 2019. Low air humidity increases aggressiveness of ixodid ticks (Acari: ixodidae) under high ambient temperatures (a preliminary hypothesis). Ticks Tick-borne Dis 10: 101274.

    • Search Google Scholar
    • Export Citation
  • 27.

    Papa A, Chaligiannis I, Xanthopoulou K, Papaioakim M, Papanastasiou S, Sotiraki S., 2010. Ticks parasitizing humans in Greece. Vector-borne Zoonotic Dis 11: 539542.

    • Search Google Scholar
    • Export Citation
  • 28.

    Karl TR, Melillo JM, Peterson TC, Hassol SJ, eds., 2009. Global Climate Change Impacts in the United States. New York, NY: Cambridge University Press.

    • Search Google Scholar
    • Export Citation
  • 29.

    Black WC, Piesman J, 1994. Phylogeny of hard- and soft-tick taxa (Acari: ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci U S A 91: 1003410038.

    • Search Google Scholar
    • Export Citation
  • 30.

    Dallas T, Foré S, 2013. Chemical attraction of Dermacentor variabilis ticks parasitic to Peromyscus leucopus based on host body mass and sex. Exp Appl Acarol 61: 243250.

    • Search Google Scholar
    • Export Citation
  • 31.

    Mears S, Clark F, Greenwood M, Larsen KS, 2002. Host location, survival and fecundity of the Oriental rat flea Xenopsylla cheopis (Siphonaptera: pulicidae) in relation to black rat Rattus rattus (Rodentia: Muridae) host age and sex. Bull Entomol Res 92: 375384.

    • Search Google Scholar
    • Export Citation
  • 32.

    Bates D, Machler M, Bolker B, Walker S, 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67: 148.

  • 33.

    Koch HG, Tuck MD, 1986. Molting and survival of the brown dog tick (Acari: ixodidae) under different temperatures and humidities. Ann Entomol Soc Am 79: 1114.

    • Search Google Scholar
    • Export Citation
  • 34.

    Paz GF, Labruna MB, Leite RC, 2008. Drop off rhythm of Rhipicephalus sanguineus (Acari: ixodidae) of artificially infested dogs. Rev Bras Parasitol Veterinária 17: 139144.

    • Search Google Scholar
    • Export Citation
  • 35.

    Harrison B, Engber B, Apperson C, 1997. Ticks (Acari: ixodida) uncommonly found biting humans in North Carolina. J Vector Ecol 22: 612.

  • 36.

    Nelson VA, 1969. Human Parasitism by the brown dog tick. J Econ Entomol 62: 710712.

  • 37.

    Gilot B, Laforge ML, Pichot J, Raoult D, 1990. Relationships between the Rhipicephalus sanguineus complex ecology and mediterranean spotted fever epidemiology in France. Eur J Epidemiol 6: 357362.

    • Search Google Scholar
    • Export Citation
  • 38.

    Mentz MB, Trombka M, Silva da GL, Silva CE, 2016. Rhipicephalus sanguineus (Acari: ixodidae) biting a human being in Porto Alegre city, Rio Grande do Sul, Brazil. Rev Inst Med Trop São Paulo 58: 35.

    • Search Google Scholar
    • Export Citation
  • 39.

    Rodríguez-Vivas RI, Apanaskevich DA, Ojeda-Chi MM, Trinidad-Martínez I, Reyes-Novelo E, Esteve-Gassent MD, Pérez de León AA, 2016. Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico. Vet Parasitol 215: 106113.

    • Search Google Scholar
    • Export Citation
  • 40.

    Venzal JM, Guglielmone AA, Estrada Peña A, Cabrera PA, Castro O, 2003. Ticks (ixodida: ixodidae) parasitising humans in Uruguay. Ann Trop Med Parasitol 97: 769772.

    • Search Google Scholar
    • Export Citation
  • 41.

    Bermúdez C, Sergio E, Castro A, Esser H, Liefting Y, García G, Miranda RJ, 2012. Ticks (ixodida) on humans from central Panama, Panama (2010–2011). Exp Appl Acarol 58: 8188.

    • Search Google Scholar
    • Export Citation
  • 42.

    Carpenter TL, McMeans MC, McHugh CP, 1990. Additional instances of human parasitism by the brown dog tick (Acari: ixodidae). J Med Entomol 27: 10651066.

    • Search Google Scholar
    • Export Citation
  • 43.

    Dantas-Torres F, Latrofa MS, Annoscia G, Giannelli A, Parisi A, Otranto D, 2013. Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the new and old worlds. Parasit Vectors 6: 213.

    • Search Google Scholar
    • Export Citation
  • 44.

    Nava S, Estrada-Peña A, Petney T, Beati L, Labruna MB, Szabó MPJ, Venzal JM, Mastropaolo M, Mangold AJ, Guglielmone AA, 2015. The taxonomic status of Rhipicephalus sanguineus (Latreille, 1806). Vet Parasitol 208: 28.

    • Search Google Scholar
    • Export Citation
  • 45.

    Arenas EE, Creus BF, Cueto FB, Porta FS, 1986. Climatic factors in resurgence of Mediterranean spotted fever. Lancet 327: 1333.

  • 46.

    Raoult D, Dupont HT, Caraco P, Brouqui P, Drancourt M, Charrel C, 1992. Mediterranean spotted fever in Marseille: descriptive epidemiology and the influence of climatic factors. Eur J Epidemiol 8: 192197.

    • Search Google Scholar
    • Export Citation
  • 47.

    Dantas-Torres F, 2010. Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors 3: 26.

  • 48.

    Traeger MS 2015. Rocky Mountain spotted fever characterization and comparison to similar illnesses in a highly endemic area—Arizona, 2002–2011. Clin Infect Dis 60: 16501658.

    • Search Google Scholar
    • Export Citation
  • 49.

    Dalton MJ, Clarke MJ, Holman RC, Krebs JW, Fishbein DB, Olson JG, Childs JE, 1995. National surveillance for Rocky Mountain spotted fever, 1981–1992: epidemiologic summary and evaluation of risk factors for fatal outcome. Am J Trop Med Hyg 52: 405413.

    • Search Google Scholar
    • Export Citation
  • 50.

    Holman RC, McQuiston JH, Haberling DL, Cheek JE, 2009. Increasing incidence of Rocky Mountain spotted fever among the American Indian population in the United States. Am J Trop Med Hyg 80: 601605.

    • Search Google Scholar
    • Export Citation
  • 51.

    Raghavan RK, Goodin DG, Neises D, Anderson GA, Ganta RR, 2016. Hierarchical bayesian spatio–temporal analysis of climatic and socio–economic determinants of Rocky Mountain spotted fever. PLoS One 11: e0150180.

    • Search Google Scholar
    • Export Citation
  • 52.

    Arsnoe I, Tsao JI, Hickling GJ, 2019. Nymphal Ixodes scapularis questing behavior explains geographic variation in Lyme borreliosis risk in the eastern United States. Ticks Tick-borne Dis 10: 553563.

    • Search Google Scholar
    • Export Citation
  • 53.

    Elizarov I, Vasiuta A, 1976. Distance orientation of the tick Ixodes persulcatus to the attractant factors of the prey. Parazitologiia 10: 136141.

    • Search Google Scholar
    • Export Citation
  • 54.

    Waladde SM, Rice MJ, 1982. The sensory basis of tick feeding behaviour. Obenchain FD, Galun R, eds. Physiology of Ticks. Elmsford, NY: Pergamon, 71118.

    • Search Google Scholar
    • Export Citation
  • 55.

    Webb JP, 1979. Host-locating behavior of nymphal Ornithodoros concanensis (acarina: Argasidae). J Med Entomol 16: 437447.

  • 56.

    Perritt DW, Couger G, Barker RW, 1993. Computer-controlled olfactometer system for studying behavioral responses of ticks to carbon dioxide. J Med Entomol 30: 571578.

    • Search Google Scholar
    • Export Citation
  • 57.

    de Oliveira Filho JG, Sarria ALF, Ferreira LL, Caulfield JC, Powers SJ, Pickett JA, de León AAP, Birkett MA, Borges LMF, 2016. Quantification of brown dog tick repellents, 2-hexanone and benzaldehyde, and release from tick-resistant beagles, Canis lupus familiaris. J Chromatogr B 1022: 6469.

    • Search Google Scholar
    • Export Citation
  • 58.

    Louly CCB, Soares SF, Silveira DN, Neto OJS, Silva AC, Borges LMF, 2009. Differences in the susceptibility of two breeds of dogs, english cocker spaniel and beagle, to Rhipicephalus sanguineus (Acari: ixodidae). Int J Acarol 35: 2532.

    • Search Google Scholar
    • Export Citation
  • 59.

    Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E, 2009. Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip Perspect Infect Dis 2009: 593232.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Effect of Temperature on Host Preference in Two Lineages of the Brown Dog Tick, Rhipicephalus sanguineus

View More View Less
  • 1 Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, Davis, California

Abstract.

Rhipicephalus sanguineus is a species complex of ticks that vector disease worldwide. Feeding primarily on dogs, members of the complex also feed incidentally on humans, potentially transmitting disease agents such as Rickettsia rickettsii, Rickettsia conorii, and Ehrlichia species. There are two genetic Rh. sanguineus lineages in North America, designated as the temperate and tropical lineages, which had occurred in discrete locations, although there is now range overlap in parts of California and Arizona. Rh. sanguineus in Europe are reportedly more aggressive toward humans during hot weather, increasing the risk of pathogen transmission to humans. The aim of this study was to assess the impact of hot weather on choice between humans and dog hosts among tropical and temperate lineage Rh. sanguineus individuals. Ticks in a two-choice olfactometer migrated toward a dog or human in trials at room (23.5°C) or high temperature (38°C). At 38°C, 2.5 times more tropical lineage adults chose humans compared with room temperature, whereas temperate lineage adults demonstrated a 66% reduction in preference for dogs and a slight increase in preference for humans. Fewer nymphs chose either host at 38°C than at room temperature in both lineages. These results demonstrate that risk of disease transmission to humans may be increased during periods of hot weather, where either lineage is present, and that hot weather events associated with climatic change may result in more frequent rickettsial disease outbreaks.

Author Notes

Address correspondence to Laura H. Backus, Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, 1320 Tupper Hall, Davis, CA 95616. E-mail: lhbackus@ucdavis.edu

Financial support: This research was funded through support of the Pacific Southwest Regional Center of Excellence for Vector-Borne Diseases, funded by the U.S. Centers for Disease Control and Prevention (Cooperative agreement 1U01CK000516).

Authors’ addresses: Laura H. Backus, Andrés M. López Pérez, and Janet E. Foley, Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, Davis, CA, E-mails: lhbackus@ucdavis.edu, amlope@ucdavis.edu, and jefoley@ucdavis.edu.

Save