Bat ecology and public health surveillance for rabies in an urbanizing region of Colorado

Urban Ecosystems

Volumn 14, Issue 4, 2011, Pages 665-697

  O'Shea, Thomas J ^a   Neubaum, Daniel J ^b   Neubaum, Melissa A ^b   Cryan, Paul M ^a   Ellison, Laura E ^a   Stanley, Thomas R ^a   Rupprecht, Charles E ^c   Pape, W John ^d   Bowen, Richard A ^b  

^a FORT COLLINS SCIENCE CENTER   (United States)

^b Veterinary Dentistry and Oral Surgery   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d Air Pollution Control Division   (United States)

Author keywords

Bats; Big brown bats; Chiroptera; Disease; Public health; Rabies

Indexed keywords

CHIROPTERA; EPTESICUS; EPTESICUS FUSCUS;

EID: 82655182035     PISSN: 10838155     EISSN: 15731642     Source Type: Journal    
DOI: 10.1007/s11252-011-0182-7     Document Type: Article

References (101)

1. Adams CE, Lindsey KJ, Ash SJ (2006) Urban wildlife management. CRC Taylor & Francis, Boca Raton.
2. Aldridge HDJN, Brigham RM (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% "rule" of radio-telemetry. J Mammal 69: 379-382.
3. Anderson DR, Burnham KP, Thompson WL (2000) Null hypothesis testing: problems, prevalence, and an alternative. J Wildl Manag 64: 912-923.
4. Anderson DR, Link WA, Johnson DH, Burnham KP (2001) Suggestions for presenting the results of data analyses. J Wildl Manag 65: 373-378.
5. Anthony ELP (1988) Age determination in bats. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats. Smithsonian Institution, Washington, DC, pp 47-58.
6. Arbor Day Foundation (2009) What is Tree City USA? In: Arbor Day Foundation. http://www. arborday. org/index. cfm. Accessed 18 May 2009.
7. Armstrong DM (1972) Distribution of mammals in Colorado. Monogr Mus Nat Hist, Univ Kansas 3: 1-415.
8. Armstrong DM, Adams RA, Freeman J (1994) Distribution and ecology of bats of Colorado. Nat Hist Invent Colo, Univ Colo Mus 15: 1-83.
9. Blanton JD, Hanlon CA, Rupprecht CE (2007) Rabies surveillance in the United States during 2006. J Am Vet Med Assoc 231: 540-556.
10. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323: 227.
11. Bode AV, Sejvar JJ, Pape WJ, Campbell GL, Marfin AA (2006) West Nile virus disease: a descriptive study of 228 patients hospitalized in a 4-county region of Colorado in 2003. Clin Infect Dis 42: 1234-1240.
12. Bolling BG, Moore CG, Anderson SL, Blair CD, Beaty BJ (2007) Entomological studies along the Colorado Front Range during a period of intense West Nile virus activity. J Am Mosq Control Assoc 23: 37-46.
13. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trend Ecol Evol 22: 95-102.
14. Brigham RM (1991) Flexibility in foraging and roosting behaviour by the big brown bat (Eptesicus fuscus). Can J Zool 69: 117-121.
15. Brigham RM, Fenton MB (1986) The influence of roost closure on the roosting and foraging behaviour of Eptesicus fuscus (Chiroptera: Vespertilionidae). Can J Zool 64: 1128-1133.
16. Bunde JM, Heske EJ, Mateus-Pinilla NE, Hofmann JE, Novak RJ (2006) A survey for West Nile virus in bats from Illinois. J Wildl Dis 42: 455-458.
17. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York.
18. Calisher CH, Holmes KV, Dominguez SR, Schountz T, Cryan P (2008) Bats prove to be rich reservoirs for emerging viruses. Microbe 3: 521-528.
19. Centers for Disease Control and Prevention (1999) Human rabies prevention - United States, 1999 recommendations of the Advisory Committee on Immunization Practices (ACIP). Morb and Mortal Wkly Rep 48 (RR-1): 1-21.
20. City of Fort Collins (1996) Geographic information services division. City of Fort Collins, Colorado USA. http://www. ci. fort-collins. co. us/gis. Accessed 22 April 2003.
21. City of Fort Collins (2006a) General population characteristics. In: Trends 2004. City of Fort Collins. http://www. fcgov. com/advanceplanning/trends. php. Accessed 4 October 2006.
22. City of Fort Collins (2006b) Local history archive. http://library. ci. fort-collins. co. us/ Local_history/Topics/contexts/table1. htm. Accessed 4 October 2006.
23. Clark DR Jr, Shore RF (2001) Chiroptera. In: Shore RF, Rattner BA (eds) Ecotoxicology of wild mammals. John Wiley & Sons, New York, pp 159-214.
24. Colorado Department of Public Health and Environment (2009) Population, population growth (2003-2004), and population density by county and region: Colorado residents, 2004. http://www. cdphe. state. co. us/hs/vs/2004/p6. pdf Accessed 28 April 2009.
25. Colorado State University (2006) Colorado climate center. http://ccc. atmos. colostate. edu. Accessed 4 October 2006.
26. Cryan PM, Bogan MA, Yanega GM (2001) Roosting habits of four bat species in the Black Hills of South Dakota. Acta Chiropt 3: 43-52.
27. Davis A, Bunning M, Gordy P, Panella N, Blitvich B, Bowen RA (2005) Experimental and natural infection of North American bats with West Nile virus. Amer J Trop Med Hyg 73: 467-469.
28. De Serres G, Dallaire F, Côte M, Skowronski DM (2008) Bat rabies in the United States and Canada from 1950 through 2007: human cases with and without bat contact. Clin Infect Dis 46: 1329-1337.
29. Duchamp JE, Sparks DW, Whitaker JO Jr (2004) Foraging-habitat selection by bats at an urban-rural interface: comparison between a successful and a less successful species. Can J Zool 82: 1157-1164.
30. Duerksen CJ, Snyder C (2005) Nature-friendly communities: habitat protection and land use. Island, Washington DC.
31. Ellison LE, O'Shea TJ, Neubaum DJ, Bowen RA (2007a) Factors influencing movement probabilities of big brown bats (Eptesicus fuscus) in buildings. Ecol Appl 17: 620-627.
32. Ellison LE, O'Shea TJ, Neubaum DJ, Neubaum MA, Pearce RD, Bowen RA (2007b) A comparison of conventional capture versus PIT reader techniques for estimating survival and capture probabilities of big brown bats (Eptesicus fuscus). Acta Chiropt 9: 149-160.
33. Evelyn MJ, Stiles DA, Young RA (2004) Conservation of bats in suburban landscapes: roost selection by Myotis yumanensis in a residential area in California. Biol Conserv 115: 463-473.
34. Everette AL, O'Shea TJ, Ellison LE, Stone LA, McCance JL (2001) Bat use of a high plains urban wildlife refuge. Wildl Soc Bull 29: 967-973.
35. Faeth SH, Warren PS, Shochat E, Marussich WA (2005) Trophic dynamics in urban communities. BioScience 55: 399-407.
36. Falk JH (1976) Energetics of a suburban ecosystem. Ecology 57: 141-150.
37. Fitzgerald JP, Meaney CA, Armstrong DM (1994) Mammals of Colorado. Denver Museum of Natural History and University of Colorado Press, Boulder.
38. Fort Collins Coloradoan (2007) Online archives. http://www. coloradoan. com. Accessed 18 September 2007.
39. Franka R, Constantine DG, Kuzmin I, Velasco-Villa A, Reeder SA, Streicker D, Orciari LA, Wong AJ, Blanton JD, Rupprecht CE (2006) A new phylogenetic lineage of rabies virus associated with western pipistrelle bats (Pipistrellus hesperus). J Gen Virol 87: 2309-2321.
40. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329: 679-682.
41. Furlonger CL, Dewar HJ, Fenton MB (1987) Habitat use by foraging insectivorous bats. Can J Zool 65: 284-288.
42. Geggie JF, Fenton MB (1985) A comparison of foraging by Eptesicus fuscus (Chiroptera: Vespertilionidae) in urban and rural environments. Can J Zool 63: 263-267.
43. Gehrt SD, Chelsvig JE (2004) Species-specific patterns of bat activity in an urban landscape. Ecol Appl 14: 625-635.
44. Golubiewski NE (2006) Urbanization increases grassland carbon pools: effects of landscaping in Colorado's Front Range. Ecol Appl 16: 555-571.
45. Gujral IB, Zielinski-Gutierrez EC, LeBailly A, Nasci R (2007) Behavioral risks for West Nile Virus disease, Northern Colorado, 2003. Emerg Infect Dis 13: 419-425.
46. Humphrey SR (1975) Nursery roosts and community diversity of Nearctic bats. J Mammal 56: 321-346.
47. Jackson AC, Wunner WH (2007) Rabies, 2nd edn. Acad, New York.
48. Johnson DH (1999) The insignificance of statistical significance testing. J Wildl Manag 63: 763-772.
49. Johnson JB, Gates JE, Ford WM (2008) Distribution and activity of bats at local and landscape scales within a rural-urban gradient. Urban Ecosyst 11: 227-242.
50. Kalcounis MC, Brigham RM (1998) Secondary use of aspen cavities by tree-roosting big brown bats. J Wildl Manag 62: 603-611.
51. Kaye JP, McCulley RL, Burke IC (2005) Carbon fluxes, nitrogen cycling, and soil microbial communities in adjacent urban, native and agricultural ecosystems. Glob Change Biol 11: 575-587.
52. Knopf FL (1986) Changing landscapes and the cosmopolitism of the eastern Colorado avifauna. Wildl Soc Bull 14: 132-142.
53. Knopf FL, Scott ML (1990) Altered flows and created landscapes in the Platte River headwaters, 1840-1990. In: Sweeney JM (ed) Management of dynamic ecosystems, North Central Section. The Wildlife Society, West Lafayette, Indiana, pp 47-70.
54. Kunz TH (2003) Censusing bats: challenges, solutions, and sampling biases. In: O'Shea TJ, Bogan MA (eds) Monitoring trends in bat populations of the United States and territories: problems and prospects, US Geological Survey Information and Technology Report ITR-2003-003, pp 9-19.
55. Kunz TH, Reynolds DS (2003) Bat colonies in buildings. In: O'Shea TJ, Bogan MA (eds) Monitoring trends in bat populations of the United States and territories: problems and prospects, T. J. US Geological Survey Information and Technology Report ITR-2003-003, pp 91-102.
56. Kunz TH, Tidemann CR, Richards GC (1996) Small volant mammals. In: Wilson DE, Cole FR, Nichols JD, Rudran R, Foster MS (eds) Measuring and monitoring biological diversity: standard methods for mammals. Smithsonian Institution, Washington DC, pp 122-146.
57. Kurta A, Baker RH (1990) Eptesicus fuscus. Mamm Species 356: 1-10.
58. Kurta A, Teramino JA (1992) Bat community structure in an urban park. Ecography 15: 257-261.
59. Kuzmin IV, Rupprecht CE (2007) Bat rabies. In: Jackson AC, Wunner WH (eds) Rabies. Acad, New York, pp 259-308.
60. Lacki MJ, Hayes JP, Kurta A (eds) (2007) Bats in forests: conservation and management. Johns Hopkins University Press, Baltimore.
61. Lausen CL, Barclay RMR (2002) Roosting behavior and roost selection of female big brown bats (Eptesicus fuscus) roosting in rock crevices in southeastern Alberta. Can J Zool 80: 1069-1076.
62. Lausen CL, Barclay RMR (2003) Thermoregulation and roost selection by reproductive female big brown bats (Eptesicus fuscus) roosting in rock crevices. J Zool 260: 235-244.
63. Lechleitner RR (1969) The wild mammals of Colorado. Pruett, Boulder.
64. Loeb SC, Post CJ, Hall ST (2009) Relationship between urbanization and bat community structure in national parks of the southeastern U. S. Urban Ecosyst 12: 197-214.
65. Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton.
66. Mayrberger S (2003) Exit/entry sequences, roost fidelity and transport of young by big brown bats at a summer roost. MS Thesis. University of Michigan-Flint, Flint, MI.
67. McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93: 825-835.
68. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52: 883-890.
69. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Cons 127: 247-260.
70. Messenger SL, Smith JS, Rupprecht CE (2002) Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States. Clin Infect Dis 35: 738-747.
71. Mondul AM, Krebs JW, Childs JE (2003) Trends in national surveillance for rabies among bats in the United States (1993-2000). J Am Vet Med Assoc 222: 633-639.
72. Nams VO (1990) LOCATE II user's guide. Pacer, Truro, Nova Scotia, Canada.
73. Nemeth NM, Beckett S, Edwards E, Klenk K, Komar N (2007) Avian mortality surveillance for West Nile virus in Colorado. Amer J Trop Med Hyg 76: 431-437.
74. Neubaum DJ (2005) Records of the eastern red bat on the Northern Front Range of Colorado. Prairie Nat 37: 41-42.
75. Neubaum DJ, Andre M, Ellison LE, O'Shea TJ (2005) Survival and condition of big brown bats (Eptesicus fuscus) after radiotagging. J Mammal 86: 95-98.
76. Neubaum DJ, O'Shea TJ, Wilson KR (2006) Autumn migration and selection of rock crevices as hibernacula by big brown bats (Eptesicus fuscus) in Colorado. J Mammal 87: 470-479.
77. Neubaum DJ, Wilson KR, O'Shea TJ (2007) Urban maternity-roost selection by big brown bats in Colorado. J Wildl Manag 71: 728-736.
78. Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17: 857-872.
79. Noel TJ, Sladek RD (2002) Fort Collins & Larimer County: an illustrated history. Heritage Media, Carlsbad.
80. O'Shea TJ, Ellison LE, Stanley TR (2004) Survival estimation in bats: historical overview, critical appraisal, and suggestions for new approaches. In: Thompson WL (ed) Sampling rare or elusive species: concepts, designs, and techniques for estimating population parameters. Island, Washington, DC, pp 297-336.
81. O'Shea TJ, Ellison LE, Stanley TR (2011) Adult survival and population growth rate in Colorado big brown bats (Eptesicus fuscus). J Mammal 92: 433-443.
82. O'Shea TJ, Ellison LE, Neubaum DJ, Neubaum MA, Reynolds CA, Bowen RA (2010) Recruitment in a Colorado population of big brown bats: breeding probabilities, litter size, and first-year survival. J Mammal 91: 418-428.
83. Pape WJ, Fitzsimmons TD, Hoffman RE (1999) Risk for rabies transmission from encounters with bats, Colorado, 1977-1996. Emerg Infect Dis 5: 433-437.
84. Pilipski JD, Pilipski LM, Risley LS (2004) West Nile virus antibodies in bats from New Jersey and New York. J Wildl Dis 40: 335-337.
85. Racey PH (1988) Reproductive assessment in bats. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats. Smithsonian Institution, Washington, DC, pp 31-46.
86. SAS Institute (2003) SAS Online Doc 9. 1. SAS Institute Inc., Cary, NC.
87. Schowalter DB, Gunson JR (1979) Reproductive biology of the big brown bat (Eptesicus fuscus) in Alberta. Can Field-Nat 93: 48-54.
88. Sexton NR, Stewart SC (2007) Understanding knowledge and perceptions of bats among residents of Fort Collins, Colorado. USGS Open-File Rep 2007-1245: 1-22.
89. Shankar V, Orciari LA, De Mattos C, Kuzmin IV, Pape WJ, O'Shea TJ, Rupprecht CE (2005) Genetic divergence of rabies viruses from bat species of Colorado, USA. Vector Borne Zoonotic Dis 5: 330-341.
90. Shochat R, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From pattern to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21: 186-191.
91. Vonhof MJ, Barclay RMR (1996) Roost-site selection and roosting ecology of forest-dwelling bats in southern British Columbia. Can J Zool 74: 1797-1805.
92. Warren ER (1910) The mammals of Colorado. GP Putnam's Sons, New York.
93. Watrous A (1911) History of Larimer County, Colorado. Courier Printing and Publishing Co., Fort Collins.
94. Whitaker JO Jr, Douglas LR (2006) Bat rabies in Indiana. J Wildl Manag 70: 1569-1573.
95. Whitaker JO Jr, Gummer SL (1992) Hibernation of the big brown bat, Eptesicus fuscus, in buildings. J Mammal 73: 312-316.
96. Williams LM, Brittingham MC (1997) Selection of maternity roosts by big brown bats. J Wildl Manag 61: 359-368.
97. Willis CKR, Brigham RM (2004) Roost switching, roost sharing and social cohesion: forest-dwelling big brown bats, Eptesicus fuscus, conform to the fission-fusion model. Anim Behav 68: 495-505.
98. Willis CKR, Voss CM, Brigham RM (2006) Roost selection by forest-living female big brown bats (Eptesicus fuscus). J Mammal 87: 345-350.
99. Wimsatt J, O'Shea TJ, Ellison LE, Pearce RD, Price VR (2005) Anesthesia and blood sampling of wild big brown bats (Eptesicus fuscus) with an assessment of impacts on survival. J Wildl Dis 41: 87-95.
100. Wong S, Lau S, Woo P, Yuen K-Y (2007) Bats as a continuing source of emerging infections in humans. Rev Med Virol 17: 67-91.
101. World Health Organization (2009) Rabies. Available at http://www. who. int/mediacentre/ factsheets/fs099/en/index. html. Accessed 4 June 2009.