Dispatch MMWR, 2006. Human Plague—Four States, 2006. Morbidity and Mortality Weekly Report. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5534a4.htm. Accessed August 25, 2006.
Gage KL, Kosoy MY, 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505–528.
Perry R, Fetherston J, 1997. Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev 10: 35–66.
Tikhomirov E, 1999. Epidemiology and distribution of plague. Plague Manual: Epidemiology, Distribution, Surveillance, and Control. Dennis DT, Gage KL, Gratz NG, Poland JD, Tikhomirov E, eds. Geneva: World Health Organization; 63–96.
McNabb SJ, Jajosky RA, Hall-Baker PA, Adams D, Sharp P, Worshams C, Anderson WJ, Javier AJ, Jones GJ, Nitschke DA, Rey A, Wodajo MS, 2008. Centers for Disease Control and Prevention (CDC). Summary of notifiable diseases—United States, 2006. MMWR Morb Mortal Wkly Rep 21: 1–92.
Cully JF, Carter LG, Gage KL, 2000. New records of sylvatic plague in Kansas. Journal of Wildlife Diseases 36: 389–392.
Link VB, 1955. A History of Plague in the United States of America. Public Health Monograph. Washington, DC: US Public Health Service.
Adjemian JZ, Foley P, Gage KL, Foley JE, 2007. Initiation and spread of travelling waves of plague, Yersinia pestis, in the western United States. Am J Trop Med Hyg 76: 365–375.
Barnes AM, 1982. Surveillance and control of Bubonic plague in the United States. Symp Zool Soc Lond 50: 257–275.
Anderson ET, 1978. Plague in the continental United States, 1900–76. Public Health Rep 93: 297–301.
Stenseth NC, Samia NI, Viljugrein H, Kausrud KL, Begon M, Davis S, Leirs H, Dubyanskiy VM, Esper J, Ageyev VS, Klassovskiy NL, Pole SB, Chan KS, 2006. Plague dynamics are driven by climate variation. Proc Natl Acad Sci USA 103: 13110–13115.
WHO (World Health Organization), 2003. Plague. Wkly Epidemiol Rec 78: 253–260.
WHO (World Health Organization), 2005. Plague. Wkly Epidemiol Rec 80: 138–140.
Davis S, Leirs H, Viljugrein H, Stenseth NC, De Bruyn L, Klassovskiy N, Ageyev V, Begon M, 2005. Empirical assessment of a threshold model for sylvatic plague. J R Soc Interface 4: 649–657.
Jaksic FM, Lima M, 2003. Myths and facts on ratadas: bamboo blooms, rainfall peaks and rodent outbreaks in South America. Aust J Ecol 28: 237–251.
Leirs H, Verhagen R, Verheyen W, Mwanjabe P, Mbise T, 1996. Forecasting rodent outbreaks in Africa: an ecological basis for Mastomys control in Tanzania. J Appl Ecol 33: 937–943.
Lima M, Jaksic FM, 1999. Population rate of change in the leaf-eared mouse: the role of density-dependence, seasonality and rainfall. Aust J Ecol 24: 110–116.
Lima M, Jaksic FM, 1999. Population dynamics of three neotropical small mammals: time series models and the role of delayed density-dependence in population irruptions. Aust J Ecol 24: 25–34.
Lima M, Keymer JE, Jaksic FM, 1999. El Nino-southern oscillation-driven rainfall variability and delayed density dependence cause rodent outbreaks in western South America: linking demography and population dynamics. Am Nat 153: 476–491.
Stapp P, Antolin MF, Ball M, 2004. Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Nino events. Front Ecol Environ 2: 235–240.
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV, 2001. Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Med Vet Entomol 15: 249–258.
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV, 2001. Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38: 629–637.
Gage KL, Burkot TR, Eisen RJ, Hayes EB, 2008. Climate and vector borne diseases. Am J Prev Med 35: 436–450.
Tripp DW, Gage KL, Montenieri JA, Antolin MF, 2009. Flea abundance on black-tailed prairie dogs (Cynomys ludovicianus) increases during plague epizootics. Vector Borne Zoonotic Dis 9: 313–321.
Anderson RM, May RM, 1991. Infectious Disease of Humans—Dynamics and Control. Oxford, UK: Oxford University Press.
Davis S, Begon M, De Bruyn L, Ageyev VS, Klassovskiy NL, Pole SB, Viljugrein H, Stenseth NC, Leirs H, 2004. Predictive thresholds for plague in Kazakhstan. Science 304: 736–738.
Hudson PJ, Rizzoli AP, Grenfell BT, Heesterbeek JAP, Dobson AP, 2002. Ecology of wildlife diseases. The Ecology of Wildlife Disease. Oxford, UK: Oxford University Press.
Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RE, Reynolds PJ, Engelthaler DM, Levy CE, Parmenter RR, Montenieri JA, Cheek JE, Grinnell RK, Ettestad PJ, Gage KL, 2002. Modeling relationships between climate and the frequency of human plague cases in the southwestern United States. Am J Trop Med Hyg 66: 186–196.
Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL, 1999. Incidence of plague associated with increased winter-spring precipitation in New Mexico. Am J Trop Med Hyg 61: 814–821.
Collinge S, Johnson W, Ray C, Matchett R, Grensten J, Cully J Jr, Gage K, Kosoy M, Loye J, Martin A, 2005. Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecol 20: 941–955.
Duplantier J-M, Duchemin J-B, Chanteau S, Carniel E, 2005. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res 36: 437–453.
Eisen RJ, Glass GE, Eisen L, Cheek J, Enscore RE, Ettestad P, Gage KL, 2007. A spatial model of shared risk for plague and hantavirus pulmonary syndrome in the southwestern United States. Am J Trop Med Hyg 77: 999–1004.
Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, Patz JA, 2001. Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases. Environ Health Perspect 109: 223–233.
Kolivras KN, Comrie AC, 2004. Climate and infectious disease in the southwestern United States. Prog Phys Geogr 28: 387–398.
Kovats RS, Bouma MJ, Hajat S, Worrall E, Haines A, 2003. El Nino and health. Lancet 362: 1481–1489.
Nakazawa Y, Williams R, Peterson AT, Mead P, Staples E, Gage KL, 2007. Climate change effects on plague and tularemia in the United States. Vector Borne Zoonotic Dis 7: 529–540.
Mantua NJ, Hare SR, 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78: 1069–1079.
McCreary JP, 1986. Coupled ocean–atmosphere model of El Niño and the Southern Oscillation. Willebrand J, Anderson DLT, eds. Oceans and Atmospheres, 247–280.
Holmgren M, Scheffer M, Ezcurra E, Gutiérrez JR, Mohren GMJ, 2001. El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16: 89–94.
Ben Ari T, Gershunov A, Gage KL, Snäll T, Ettestad P, Kausrud KL, Stenseth NC, 2008. Human plague in the USA: the importance of regional and local climate. Biol Lett 4: 737–740.
Diaz HF, 1992. Atmospheric teleconnections associated with the extreme phase of the Southern Oscillation. Diaz HF, Markgraf V, eds. El Niño: Historical and Paleoclimatic Aspects of the Southern Oscillation. Cambridge, UK: Cambridge University Press, 7–28.
Gershunov A, Barnett TP, 1998. Interdecadal modulation of ENSO teleconnections. Bull Am Meteorol Soc 79: 2715–2725.
Hallett TB, Coulson T, Pilkington JG, Clutton-Brock TH, Pemberton JM, Grenfell BT, 2004. Why large-scale climate indices seem to predict ecological processes better than local weather. Nature 430: 71–75.
Stenseth NC, Mysterud A, 2005. Weather packages: finding the right scale and composition of climate in ecology. J Anim Ecol 74: 1195–1198.
Barnett TP, Pierce DW, Hidalgo HG, Bonfils C, Santer BD, Das T, Bala G, Wood AW, Nozawa T, Mirin AA, Cayan DR, Dettinger MD, 2008. Human-induced changes in the hydrology of the western United States. Science 319: 1080–1083.
Stapp P, 2007. Rodent communities in active and inactive colonies of black-tailed prairie dogs in shortgrass steppe. J Mammal 88: 241–249.
Holmgren M, Scheffer M, Ezcurra E, Gutiérrez JR, Mohren GMJ, 2001. El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16: 89–94.
Letnic M, Tamayo B, Dickman CR, 2005. The responses of mammals to La Nina (El Nino Southern Oscillation)-associated rainfall, predation, and wildfire in central Australia. J Mammal 86: 689–703.
Forrest GH, Collatz G, Los S, Brown de Colstoun E, Landis D, 2005. ISLSCP Initiative II Data Archive. NASA.
Cazelles B, Chavez M, McMichael AJ, Hales S, 2005. Nonstationary influence of El Niño on the synchronous dengue epidemics in Thailand. PLoS Med 2: 313–318.
Cazelles B, Hales S, 2006. Infectious diseases, climate influences and nonstationary. PLoS Med 3: 1212–1213.
Hastings A, 2001. Transient dynamics and persistence of ecological systems. Ecol Lett 4: 215–220.
Stenseth NC, Falck W, Chan K-S, Bjørnstad ON, O'Donoghue M, Tong H, Boonstra R, Boutin S, Krebs CJ, Yoccozaj NG, 1998. From patterns to processes: phase and density dependencies in the Canadian lynx cycle. Proc Natl Acad Sci USA 95: 15430–15435.
Cazelles B, Chavez M, Magny GC, Guégan J-F, Hales S, 2007. Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface 4: 625–636.
Cazelles B, Chavez M, Berteaux D, Ménard F, Vik J, Jenouvrier S, Stenseth N, 2008. Wavelet analysis of ecological time series. Oecologia 156: 287–304.
Daubechies L, 1992. Ten Lectures on Wavelets. SIAM. Available at: http://www.ec-securehost.com/SIAM/CB61.html.
Lau K, Weng H, 1995. Climate signal detection using wavelet transform: how to make a time series sing. Bull Am Meteorol Soc 76: 2391–2402.
Torrence C, Compo GP, 1998. A practical guide to wavelet analysis. Bull Am Meteorol Soc 79: 61–78.
Rouyer T, Fromentin J-M, Stenseth NC, Cazelles B, 2008. Analysing multiple time series and extending significance testing in wavelet analysis. Mar Ecol Prog Ser 359: 11–23.
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Kausrud KL, Viljugrein H, Frigessi A, Begon M, Davis S, Leirs H, Dubyanskiy V, Stenseth NC, 2007. Climatically driven synchrony of gerbil populations allows large-scale plague outbreaks. Proc R Soc Lond B Biol Sci 274: 1963–1969.
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Plague is a vector-borne, highly virulent zoonotic disease caused by the bacterium Yersinia pestis. It persists in nature through transmission between its hosts (wild rodents) and vectors (fleas). During epizootics, the disease expands and spills over to other host species such as humans living in or close to affected areas. Here, we investigate the effect of large-scale climate variability on the dynamics of human plague in the western United States using a 56-year time series of plague reports (1950–2005). We found that El Niño Southern Oscillation and Pacific Decadal Oscillation in combination affect the dynamics of human plague over the western United States. The underlying mechanism could involve changes in precipitation and temperatures that impact both hosts and vectors. It is suggested that snow also may play a key role, possibly through its effects on summer soil moisture, which is known to be instrumental for flea survival and development and sustained growth of vegetation for rodents.
Authors' addresses: Tamara Ben Ari, Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Oslo, Norway, and Ecole Normale Superieure, Paris, France. Alexander Gershunov, Climate Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, E-mail: sasha@ucsd.edu. Rouyer Tristan, Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Oslo, Norway, E-mail: rouyer.tristan@bio.uio.no. Bernard Cazelles, Ecole Normale Superieure, Paris, France, E-mail: cazelles@biologie.ens.fr. Kenneth Gage, Bacterial Zoonoses Branch, Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, E-mail: klg0@cdc.gov. Nils Chr. Stenseth, Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Oslo, Norway, E-mail: n.c.stenseth@bio.uio.no.
Dispatch MMWR, 2006. Human Plague—Four States, 2006. Morbidity and Mortality Weekly Report. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5534a4.htm. Accessed August 25, 2006.
Gage KL, Kosoy MY, 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505–528.
Perry R, Fetherston J, 1997. Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev 10: 35–66.
Tikhomirov E, 1999. Epidemiology and distribution of plague. Plague Manual: Epidemiology, Distribution, Surveillance, and Control. Dennis DT, Gage KL, Gratz NG, Poland JD, Tikhomirov E, eds. Geneva: World Health Organization; 63–96.
McNabb SJ, Jajosky RA, Hall-Baker PA, Adams D, Sharp P, Worshams C, Anderson WJ, Javier AJ, Jones GJ, Nitschke DA, Rey A, Wodajo MS, 2008. Centers for Disease Control and Prevention (CDC). Summary of notifiable diseases—United States, 2006. MMWR Morb Mortal Wkly Rep 21: 1–92.
Cully JF, Carter LG, Gage KL, 2000. New records of sylvatic plague in Kansas. Journal of Wildlife Diseases 36: 389–392.
Link VB, 1955. A History of Plague in the United States of America. Public Health Monograph. Washington, DC: US Public Health Service.
Adjemian JZ, Foley P, Gage KL, Foley JE, 2007. Initiation and spread of travelling waves of plague, Yersinia pestis, in the western United States. Am J Trop Med Hyg 76: 365–375.
Barnes AM, 1982. Surveillance and control of Bubonic plague in the United States. Symp Zool Soc Lond 50: 257–275.
Anderson ET, 1978. Plague in the continental United States, 1900–76. Public Health Rep 93: 297–301.
Stenseth NC, Samia NI, Viljugrein H, Kausrud KL, Begon M, Davis S, Leirs H, Dubyanskiy VM, Esper J, Ageyev VS, Klassovskiy NL, Pole SB, Chan KS, 2006. Plague dynamics are driven by climate variation. Proc Natl Acad Sci USA 103: 13110–13115.
WHO (World Health Organization), 2003. Plague. Wkly Epidemiol Rec 78: 253–260.
WHO (World Health Organization), 2005. Plague. Wkly Epidemiol Rec 80: 138–140.
Davis S, Leirs H, Viljugrein H, Stenseth NC, De Bruyn L, Klassovskiy N, Ageyev V, Begon M, 2005. Empirical assessment of a threshold model for sylvatic plague. J R Soc Interface 4: 649–657.
Jaksic FM, Lima M, 2003. Myths and facts on ratadas: bamboo blooms, rainfall peaks and rodent outbreaks in South America. Aust J Ecol 28: 237–251.
Leirs H, Verhagen R, Verheyen W, Mwanjabe P, Mbise T, 1996. Forecasting rodent outbreaks in Africa: an ecological basis for Mastomys control in Tanzania. J Appl Ecol 33: 937–943.
Lima M, Jaksic FM, 1999. Population rate of change in the leaf-eared mouse: the role of density-dependence, seasonality and rainfall. Aust J Ecol 24: 110–116.
Lima M, Jaksic FM, 1999. Population dynamics of three neotropical small mammals: time series models and the role of delayed density-dependence in population irruptions. Aust J Ecol 24: 25–34.
Lima M, Keymer JE, Jaksic FM, 1999. El Nino-southern oscillation-driven rainfall variability and delayed density dependence cause rodent outbreaks in western South America: linking demography and population dynamics. Am Nat 153: 476–491.
Stapp P, Antolin MF, Ball M, 2004. Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Nino events. Front Ecol Environ 2: 235–240.
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV, 2001. Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Med Vet Entomol 15: 249–258.
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV, 2001. Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38: 629–637.
Gage KL, Burkot TR, Eisen RJ, Hayes EB, 2008. Climate and vector borne diseases. Am J Prev Med 35: 436–450.
Tripp DW, Gage KL, Montenieri JA, Antolin MF, 2009. Flea abundance on black-tailed prairie dogs (Cynomys ludovicianus) increases during plague epizootics. Vector Borne Zoonotic Dis 9: 313–321.
Anderson RM, May RM, 1991. Infectious Disease of Humans—Dynamics and Control. Oxford, UK: Oxford University Press.
Davis S, Begon M, De Bruyn L, Ageyev VS, Klassovskiy NL, Pole SB, Viljugrein H, Stenseth NC, Leirs H, 2004. Predictive thresholds for plague in Kazakhstan. Science 304: 736–738.
Hudson PJ, Rizzoli AP, Grenfell BT, Heesterbeek JAP, Dobson AP, 2002. Ecology of wildlife diseases. The Ecology of Wildlife Disease. Oxford, UK: Oxford University Press.
Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RE, Reynolds PJ, Engelthaler DM, Levy CE, Parmenter RR, Montenieri JA, Cheek JE, Grinnell RK, Ettestad PJ, Gage KL, 2002. Modeling relationships between climate and the frequency of human plague cases in the southwestern United States. Am J Trop Med Hyg 66: 186–196.
Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL, 1999. Incidence of plague associated with increased winter-spring precipitation in New Mexico. Am J Trop Med Hyg 61: 814–821.
Collinge S, Johnson W, Ray C, Matchett R, Grensten J, Cully J Jr, Gage K, Kosoy M, Loye J, Martin A, 2005. Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecol 20: 941–955.
Duplantier J-M, Duchemin J-B, Chanteau S, Carniel E, 2005. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res 36: 437–453.
Eisen RJ, Glass GE, Eisen L, Cheek J, Enscore RE, Ettestad P, Gage KL, 2007. A spatial model of shared risk for plague and hantavirus pulmonary syndrome in the southwestern United States. Am J Trop Med Hyg 77: 999–1004.
Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, Patz JA, 2001. Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases. Environ Health Perspect 109: 223–233.
Kolivras KN, Comrie AC, 2004. Climate and infectious disease in the southwestern United States. Prog Phys Geogr 28: 387–398.
Kovats RS, Bouma MJ, Hajat S, Worrall E, Haines A, 2003. El Nino and health. Lancet 362: 1481–1489.
Nakazawa Y, Williams R, Peterson AT, Mead P, Staples E, Gage KL, 2007. Climate change effects on plague and tularemia in the United States. Vector Borne Zoonotic Dis 7: 529–540.
Mantua NJ, Hare SR, 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78: 1069–1079.
McCreary JP, 1986. Coupled ocean–atmosphere model of El Niño and the Southern Oscillation. Willebrand J, Anderson DLT, eds. Oceans and Atmospheres, 247–280.
Holmgren M, Scheffer M, Ezcurra E, Gutiérrez JR, Mohren GMJ, 2001. El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16: 89–94.
Ben Ari T, Gershunov A, Gage KL, Snäll T, Ettestad P, Kausrud KL, Stenseth NC, 2008. Human plague in the USA: the importance of regional and local climate. Biol Lett 4: 737–740.
Diaz HF, 1992. Atmospheric teleconnections associated with the extreme phase of the Southern Oscillation. Diaz HF, Markgraf V, eds. El Niño: Historical and Paleoclimatic Aspects of the Southern Oscillation. Cambridge, UK: Cambridge University Press, 7–28.
Gershunov A, Barnett TP, 1998. Interdecadal modulation of ENSO teleconnections. Bull Am Meteorol Soc 79: 2715–2725.
Hallett TB, Coulson T, Pilkington JG, Clutton-Brock TH, Pemberton JM, Grenfell BT, 2004. Why large-scale climate indices seem to predict ecological processes better than local weather. Nature 430: 71–75.
Stenseth NC, Mysterud A, 2005. Weather packages: finding the right scale and composition of climate in ecology. J Anim Ecol 74: 1195–1198.
Barnett TP, Pierce DW, Hidalgo HG, Bonfils C, Santer BD, Das T, Bala G, Wood AW, Nozawa T, Mirin AA, Cayan DR, Dettinger MD, 2008. Human-induced changes in the hydrology of the western United States. Science 319: 1080–1083.
Stapp P, 2007. Rodent communities in active and inactive colonies of black-tailed prairie dogs in shortgrass steppe. J Mammal 88: 241–249.
Holmgren M, Scheffer M, Ezcurra E, Gutiérrez JR, Mohren GMJ, 2001. El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16: 89–94.
Letnic M, Tamayo B, Dickman CR, 2005. The responses of mammals to La Nina (El Nino Southern Oscillation)-associated rainfall, predation, and wildfire in central Australia. J Mammal 86: 689–703.
Forrest GH, Collatz G, Los S, Brown de Colstoun E, Landis D, 2005. ISLSCP Initiative II Data Archive. NASA.
Cazelles B, Chavez M, McMichael AJ, Hales S, 2005. Nonstationary influence of El Niño on the synchronous dengue epidemics in Thailand. PLoS Med 2: 313–318.
Cazelles B, Hales S, 2006. Infectious diseases, climate influences and nonstationary. PLoS Med 3: 1212–1213.
Hastings A, 2001. Transient dynamics and persistence of ecological systems. Ecol Lett 4: 215–220.
Stenseth NC, Falck W, Chan K-S, Bjørnstad ON, O'Donoghue M, Tong H, Boonstra R, Boutin S, Krebs CJ, Yoccozaj NG, 1998. From patterns to processes: phase and density dependencies in the Canadian lynx cycle. Proc Natl Acad Sci USA 95: 15430–15435.
Cazelles B, Chavez M, Magny GC, Guégan J-F, Hales S, 2007. Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface 4: 625–636.
Cazelles B, Chavez M, Berteaux D, Ménard F, Vik J, Jenouvrier S, Stenseth N, 2008. Wavelet analysis of ecological time series. Oecologia 156: 287–304.
Daubechies L, 1992. Ten Lectures on Wavelets. SIAM. Available at: http://www.ec-securehost.com/SIAM/CB61.html.
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