The Characteristics of Wild Rat (Rattus spp.) Populations from an Inner-City Neighborhood with a Focus on Factors Critical to the Understanding of Rat-Associated Zoonoses
Norway and black rats (Rattus norvegicus and Rattus rattus) are among the most ubiquitous urban wildlife species and are the source of a number of zoonotic diseases responsible for significant human morbidity and mortality in cities around the world. Rodent ecology is a primary determinant of the dynamics of zoonotic pathogens in rodent populations and the risk of pathogen transmission to people, yet many studies of rat-associated zoonoses do not account for the ecological characteristics of urban rat populations. This hinders the development of an in-depth understanding of the ecology of rat-associated zoonoses, limits comparability among studies, and can lead to erroneous conclusions. We conducted a year-long trapping-removal study to describe the ecological characteristics of urban rat populations in an inner-city neighborhood of Vancouver, Canada. The study focused on factors that might influence the ecology of zoonotic pathogens in these populations and/or our understanding of that ecology. We found that rat population density varied remarkably over short geographical distances, which could explain observed spatial distributions of rat-associated zoonoses and have implications for sampling and data analysis during research and surveillance. Season appeared to influence rat population composition even within the urban environment, which could cause temporal variation in pathogen prevalence. Body mass and bite wounds, which are often used in epidemiologic analyses as simple proxies for age and aggression, were shown to be more complex than previously thought. Finally, we found that factors associated with trapping can determine the size and composition of sampled rat population, and thus influence inferences made about the source population. These findings may help guide future studies of rats and rat-associated zoonoses.
References
[1]
Aplin KP, Chesser T, Have J (2003) Evolutionary biology of the genus Rattus: Profile of an archetypal rodent pest. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM, editors. Rats, mice and people: Rodent biology and management. Canberra: ACIAR. 487–498.
[2]
Margulis HL (1977) Rat fields, neighborhood sanitation, and rat complaints in Newark, New Jersey. Geogr Rev 67: 221–231. doi: 10.2307/214022
[3]
Clinton JM (1969) Rats in urban America. Public Health Rep 84: 1–7. doi: 10.2307/4593484
[4]
Himsworth CG, Parsons KL, Jardine C, Patrick DM (2013) Rats, cities, people, and pathogens: A systematic review and narrative synthesis of literature regarding the epidemiology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis 13: 349–359. doi: 10.1089/vbz.2012.1195
[5]
Meyer A. (2003) Urban commensal rodent control; fact or fiction? In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM, editors. Rats, mice and people: Rodent biology and management. Canberra: ACIAR. 446–450.
[6]
United Nations. (2012) World urbanization prospects: The 2011 revision. Available: http://esa.un.org/unup/index.html. Accessed 10 November 2013.
[7]
Davis S, Calvet E, Leirs H (2005) Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector Borne Zoonotic Dis 5: 305–314. doi: 10.1089/vbz.2005.5.305
[8]
Villanueva SY, Ezoe H, Baterna RA, Yanagihara Y, Muto M, et al. (2010) Serologic and molecular studies of Leptospira and leptospirosis among rats in the Philippines. Am J Trop Med Hyg 82: 889–898. doi: 10.4269/ajtmh.2010.09-0711
[9]
Scialfa E, Bolpe J, Bardon JC, Ridao G, Gentile J, et al. (2010) Isolation of Leptospira interrogans from suburban rats in Tandil, Buenos Aires, Argentina. Rev Argent Microbiol 42: 126–128.
[10]
Aviat F, Blanchard B, Michel V, Blanchet B, Branger C, et al. (2009) Leptospira exposure in the human environment in France: A survey in feral rodents and in fresh water. Com Immunol Microbiol Infect Dis 32: 463–476. doi: 10.1016/j.cimid.2008.05.004
[11]
Reeves WK, Murray KO, Meyer TE, Bull LM, Pascua RF, et al. (2008) Serological evidence of typhus group Rickettsia in a homeless population in Houston, Texas. J Vector Ecol 33: 205–207. doi: 10.3376/1081-1710(2008)33[205:seotgr]2.0.co;2
[12]
Billeter SA, Gundi VAKB, Rood MP, Kosoy MY (2011) Molecular detection and identification of Bartonella species in Xenopsylla cheopis fleas (siphonaptera: Pulicidae) collected from Rattus norvegicus rats in Los Angeles, California. Appl Environ Microbiol 77: 7850–7852. doi: 10.1128/aem.06012-11
[13]
Krojgaard LH, Villumsen S, Markussen MD, Jensen JS, Leirs H, et al. (2009) High prevalence of Leptospira spp. in sewer rats (Rattus norvegicus). Epidemiol Infect 137: 1586–1592. doi: 10.1017/s0950268809002647
[14]
Koizumi N, Muto M, Tanikawa T, Mizutani H, Sohmura Y, et al. (2009) Human leptospirosis cases and the prevalence of rats harbouring Leptospira interrogans in urban areas of Tokyo, Japan. J Med Microbiol 58: 1227–1230. doi: 10.1099/jmm.0.011528-0
[15]
Feng AYT, Himsworth C. (2013) The secret life of the city rat: A review of the ecology of urban norway and black rats (Rattus norvegicus and Rattus rattus). Urban Ecosyst DOI 10.1007/s11252-013-0305-4.
[16]
Palma RE, Polop JJ, Owen RD, Mills JN (2012) Ecology of rodent-associated hantaviruses in the southern cone of South America: Argentina, Chile, Paraguay, and Uruguay. J Wildl Dis 48: 267–281. doi: 10.7589/0090-3558-48.2.267
[17]
Olsson GE, White N, Ahlm C, Elgh F, Verlemyr AC, et al. (2002) Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8: 924–929. doi: 10.3201/eid0809.020037
[18]
Cueto GR, Cavia R, Bellomo C, Padula PJ, Suarez OV (2008) Prevalence of hantavirus infection in wild Rattus norvegicus and R. rattus populations of Buenos Aires city, Argentina. Trop Med Int Health 13: 46–51. doi: 10.1111/j.1365-3156.2007.01968.x
[19]
Easterbrook JD, Kaplan JB, Vanasco NB, Reeves WK, Purcell RH, et al. (2007) A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiol Infect 135: 1192–1199. doi: 10.1017/s0950268806007746
[20]
Psaroulaki A, Antoniou M, Toumazos P, Mazeris A, Ioannou I, et al. (2010) Rats as indicators of the presence and dispersal of six zoonotic microbial agents in Cyprus, an island ecosystem: A seroepidemiological study. Trans R Soc Trop Med Hyg 104: 733–739. doi: 10.1016/j.trstmh.2010.08.005
[21]
Davis DE (1953) The characteristics of rat populations. Q Rev Biol 28: 373–401. doi: 10.1086/399860
[22]
Agudelo-Florez P, Londono AF, Quiroz VH, Angel JC, Moreno N, et al. (2009) Prevalence of Leptospira spp. in urban rodents from a groceries trade center of Medellin, Colombia. Am J Trop Med Hyg 81: 906–910. doi: 10.4269/ajtmh.2009.09-0195
[23]
Johnson MAS, Smith H, Joseph P, Gilman RH, Bautista CT, et al. (2004) Environmental exposure and leptospirosis, Peru. Emerg Infect Dis 10: 1016–1022. doi: 10.3201/eid1006.030660
[24]
Davis DE (1949) The weight of wild brown rats at sexual maturity. J Mammal 30: 125–130. doi: 10.2307/1375259
[25]
Glass GE, Korch GW, Childs JE (1988) Seasonal and habitat differences in growth rates of wild Rattus norvegicus. J Mammal 69: 587–592. doi: 10.2307/1381350
[26]
Hickman DL, Swan M (2010) Use of a body condition score technique to assess health status in a rat model of polycystic kidney disease. J Am Assoc Lab Anim Sci 49: 155–159.
[27]
Clapperton BK (2006) A review of the current knowledge of rodent behaviour in relation to control devices. Wellington: Science & Technical Publishing, Department of Conservation. 55 p.
[28]
Barnett SA (1963) The rat: A study in behaviour. Chicago: Aldine Pub Co. 288p.
[29]
Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL (2004) Wounding: The primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70: 310–317.
[30]
de Faria MT, Calderwood MS, Athanazio DA, McBride AJA, Hartskeerl RA, et al. (2008) Carriage of Leptospira interrogans among domestic rats from an urban setting highly endemic for leptospirosis in Brazil. Acta Trop 108: 1–5. doi: 10.1016/j.actatropica.2008.07.005
[31]
Taylor PJ, Arntzen L, Hayter M, Iles M, Frean J, et al. (2008) Understanding and managing sanitary risks due to rodent zoonoses in an african city: Beyond the boston model. 3: 38–50. doi: 10.1111/j.1749-4877.2008.00072.x
[32]
Antoniou M, Psaroulaki A, Toumazos P, Mazeris A, Ioannou I, et al. (2010) Rats as indicators of the presence and dispersal of pathogens in Cyprus: Ectoparasites, parasitic helminths, enteric bacteria, and encephalomyocarditis virus. Vector Borne Zoonotic Dis 10: 867–873. doi: 10.1089/vbz.2009.0123
[33]
Smith HA (2000) Where worlds collide: Social polarization at the community level in Vancouver’s Gastown/Downtown Eastside. University of British Columbia. Available: https://circle.ubc.ca/handle/2429/10914. Accessed 31 January 2014.
[34]
Himsworth CG, Feng AYT, Parsons KL, Kerr T, Patrick DM (2013) Using experiential knowledge to understand urban rat ecology: A survey of Canadian pest control professionals. Urban Ecosyst 16: 341–351. doi: 10.1007/s11252-012-0261-4
[35]
Krebs CJ (1999) Ecological methodology. New York: Addison-Wesley Educational Publishers, Inc. 620 p.
[36]
Emlen J, Stokes A, Davis D (1949) Methods for estimating populations of brown rats in urban habitats. Ecology 30: 430–442. doi: 10.2307/1932446
[37]
Aplin KP, Brown PR, Jacob J, Krebs CJ, Singleton GR (2003) Field methods for rodent studies in Asia and the Indo-Pacific. Canberra: ACIAR. 223 p.
[38]
Nagorsen DW (2002) An identification manual to the small mammals of British Columbia. Victoria: Province of British Columbia. 165 p.
[39]
Dohoo I, Martin W, Stryhn H (2007) Veterinary epidemiologic research. Charlottetown: AVC Inc. 706 p.
[40]
Harrell FE (2001) Regression modelling strategies with applications to linear models, logistic regression, and survival analysis. New York: Springer. 568 p.
[41]
Nelson L, Clark FW (1973) Correction for sprung traps in catch/effort calculations of trapping results. J Mammal 54: 295–298. doi: 10.2307/1378903
[42]
Davis DE, Emlen JT, Stokes AW (1948) Studies on home range in the brown rat. J Mammal 29: 207–225. doi: 10.2307/1375387
[43]
Gardner Santana LC, Norris DE, Fornadel CM, Hinson ER, Klein SL, et al. (2009) Commensal ecology, urban landscapes, and their influence on the genetic characteristics of city-dwelling Norway rats (Rattus norvegicus). Mol Ecol 18: 2766–2778. doi: 10.1111/j.1365-294x.2009.04232.x
[44]
Traweger D, Travnitzky R, Moser C, Walzer C, Bernatzky G (2006) Habitat preferences and distribution of the brown rat (Rattus norvegicus berk.) in the city of Salzburg (Austria): Implications for an urban rat management. J Pest Sci 79: 113–125. doi: 10.1007/s10340-006-0123-z
[45]
Traweger D, Slotta-Bachmayr L (2005) Introducing GIS-modelling into the management of a brown rat (Rattus norvegicus berk.) (mamm. rodentia muridae) population in an urban habitat. J Pest Sci 78: 17–24. doi: 10.1007/s10340-004-0062-5
[46]
Himsworth CG, Bidulka J, Parsons KL, Feng AY, Tang P, et al. (2013) Ecology of Leptospira interrogans in Norway rats (Rattus norvegicus) in an inner-city neighborhood of Vancouver, Canada. PLoS Negl Trop Dis 7: e2270. doi: 10.1371/journal.pntd.0002270
[47]
Abramowicz KF, Rood MP, Krueger L, Eremeeva ME (2011) Urban focus of Rickettsia typhi and Rickettsia felis in Los Angeles, California. Vector Borne Zoonotic Dis 11: 979–984. doi: 10.1089/vbz.2010.0117
[48]
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, et al. (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9: 467–484. doi: 10.1111/j.1461-0248.2005.00879.x
[49]
Vanasco NB, Sequeira MD, Sequeira G, Tarabla HD (2003) Associations between Leptospiral infection and seropositivity in rodents and environmental characteristics in Argentina. Prev Vet Med 60: 227–235. doi: 10.1016/s0167-5877(03)00144-2
[50]
Villafane IE, Cavia R, Vadell MV, Suarez OV, Busch M (2013) Differences in population parameters of Rattus norvegicus in urban and rural habitats of central Argentina. Mammalia 77: 187–193. doi: 10.1515/mammalia-2012-0075
[51]
Krebs C (1999) Current paradigms of rodent population dynamics - What are we missing? In: Singleton GR, Hinds LA, Leirs H, Zhang Z, editors. Ecologically-Based Management of Rodent Pests. Canberra: ACIAR. 33–48.
[52]
Davis DE (1951) A comparison of reproductive potential of two rat populations. Ecology 32: 469–475. doi: 10.2307/1931724
[53]
Mills JN, Ksiazek TG, Peters CJ, Childs JE (1999) Long-term studies of hantavirus reservoir populations in the southwestern United States: A synthesis. Emerg Infect Dis 5: 135–142. doi: 10.3201/eid0501.990116
[54]
Tagliapietra V, Rosa R, Hauffe HC, Laakkonen J, Voutilainen L, et al. (2009) Spatial and temporal dynamics of lymphocytic choriomeningitis virus in wild rodents, northern Italy. Emerg Infect Dis 15: 1019–1025. doi: 10.3201/eid1507.01524
[55]
Glass GE, Childs JE, Korch GW, Leduc JW (1988) Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101: 459–472. doi: 10.1017/s0950268800054418
[56]
Easterbrook JD, Shields T, Klein SL, Glass GE (2005) Norway rat population in Baltimore, Maryland, 2004. Vector Borne Zoonotic Dis 5: 296–299. doi: 10.1089/vbz.2005.5.296
[57]
Vadell MV, Cavia R, Suarez OV (2010) Abundance, age structure and reproductive patterns of Rattus norvegicus and Mus musculus in two areas of the city of Buenos Aires. Int J Pest Manage 56: 327–336. doi: 10.1080/09670874.2010.499479
[58]
Leslie PH, Davis DHS (1939) An attempt to determine the absolute number of rats on a given area. J Anim Ecol 8: 94–113. doi: 10.2307/1255
[59]
Himsworth CG, Patrick DM, Mak S, Jardine CM, Tang P, et al. (2014) Carriage of Clostridium difficile by wild urban Norway rats (Rattus norvegicus) and black rats (Rattus rattus). Appl Environ Microbiol 80: 1299–1305. doi: 10.1128/aem.03609-13
[60]
Przynecania W, Gryzoni W (1969) The effect of pre-baiting on captures of rodents. Acta Theriologica 14: 267–270. doi: 10.4098/at.arch.69-20
[61]
Gurnell J (1980) The effects of pre-baiting live traps on catching woodland rodents. Acta Theriologica 25: 255–264.
[62]
Taylor KD, Hammond LE, Quy RJ (1974) The reactions of common rats to four types of live-capture trap. J Appl Ecol 22: 453–459. doi: 10.2307/2402199
[63]
Worth CB (1950) Field and laboratory observations on roof rats, Rattus rattus (linnaeus), in Florida. J Mammal 31: 293–304. doi: 10.2307/1375298
[64]
Cavia R, Ruben Cueto G, Virginia Suarez O (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape Urban Plann 90: 11–19. doi: 10.1016/j.landurbplan.2008.10.017
[65]
Barnett SA, Spencer MM (1951) Feeding, social behaviour and interspecific competition in wild rats. Behaviour 3: 229–242.
[66]
Bastos AD, Nair D, Taylor PJ, Brettschneider H, Kirsten F, et al. (2011) Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa. BMC Genet 12: 26. doi: 10.1186/1471-2156-12-26
[67]
Guan P, Huang D, He M, Shen T, Guo J, et al. (2009) Investigating the effects of climatic variables and reservoir on the incidence of hemorrhagic fever with renal syndrome in Huludao City, China: A 17-year data analysis based on structure equation model. BMC infectious diseases 9: 109. doi: 10.1186/1471-2334-9-109
[68]
Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, et al. (2006) Epidemiological trends for human plague in Madagascar during the second half of the 20th century: A survey of 20,900 notified cases. Trop Med Int Health 11: 1228–1237. doi: 10.1111/j.1365-3156.2006.01677.x
[69]
Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, et al. (2001) Climate variability and change in the United States: Potential impacts on vector- and rodent-borne diseases. Environ Health Perspect 109: 223–233. doi: 10.2307/3435012