Combined effects of atrazine and chlorpyrifos on susceptibility of the tiger salamander to ambystoma tigrinum virus

EcoHealth

Volumn 6, Issue 1, 2009, Pages 91-98

  Kerby, Jacob L ^a   Storfer, Andrew ^b  

^a W O Farber Center for Civic Leadership   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Amphibian; Disease; Multiple stressors; Pesticide; Salamander; Virus

Indexed keywords

ATRAZINE; CHLORPYRIFOS;

AMBYSTOMA TIGRINUM VIRUS; ARTICLE; ENVIRONMENTAL FACTOR; IRIDOVIRUS; LARVA; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SALAMANDER; VIRUS INFECTION; VIRUS LOAD;

AMBYSTOMA; ANIMALS; ATRAZINE; CHLORPYRIFOS; DISEASE SUSCEPTIBILITY; DNA VIRUS INFECTIONS; DRUG INTERACTIONS; HERBICIDES; INSECTICIDES; LARVA; LOGISTIC MODELS; RANAVIRUS; UNITED STATES; VIRAL LOAD; WATER POLLUTANTS, CHEMICAL;

AMBYSTOMA TIGRINUM; AMBYSTOMA TIGRINUM STEBBENSI VIRUS; AMBYSTOMA TIGRINUM VIRUS; AMPHIBIA; ANIMALIA; SALAMANDROIDEA;

EID: 70350152762     PISSN: 16129202     EISSN: 16129210     Source Type: Journal    
DOI: 10.1007/s10393-009-0234-0     Document Type: Article

References (44)

1. MG Barron KB Woodburn 1995 Ecotoxicology of chlorpyrifos Reviews of Environmental Contamination and Toxicology 144 1 93 1:CAS:528:DyaK28XhsFWmsrY%3D
2. JB Belden MJ Lydy 2000 Impact of atrazine on organophoshate insecticide Toxicity Environmental Toxicology and Chemistry 19 2266 2274 10.1897/1551-5028(2000)019<2266:IOAOOI>2.3.CO;2 1:CAS:528: DC%2BD3cXosVSqu7k%3D
3. L Berger R Speare P Daszak DE Green AA Cunningham CL Goggin R Slocombe MA Ragan AD Hyatt KR McDonald HB Hines KR Lips G Marantelli H Parkes 1998 Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America Proceedings of the National Academy of Sciences USA 95 9031 9036 10.1073/pnas.95.15.9031 1:CAS:528:DyaK1cXkvFaltbc%3D (Pubitemid 28350609)
4. AR Blaustein JM Kiesecker 2002 Complexity in conservation: lessons from the global decline of amphibian populations Ecology Letters 5 597 608 10.1046/j.1461-0248.2002.00352.x (Pubitemid 34824920)
5. MD Boone SM James 2003 Interactions of an insecticide, herbicide and natural stressors in amphibian community mesocosms Ecological Applications 13 829 841 10.1890/1051-0761(2003)013[0829:IOAIHA]2.0.CO;2
6. JL Brunner DM Schock EW Davidson JP Collins 2004 Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus Ecology 85 560 566 10.1890/02-0374
7. JL Brunner K Richards JP Collins 2005 Dose and host characteristics influence virulence of ranavirus infections Oecologia 44 399 406 10.1007/s00442-005-0093-5 (Pubitemid 41399450)
8. C Carey 2000 Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans Environmental Health Perspectives 108 143 150 10.2307/3454639
9. C Carey 1993 Hypothesis concerning the causes of the disappearance of boreal toads from the mountains of Colorado Conservation Biology 7 355 362 10.1046/j.1523-1739.1993.07020355.x
10. J Charlemagne 1979 Thymus independent anti-horse erythrocyte antibody response and suppressor T cells in the Mexican axolotl (Amphibia, Urodela, Ambystoma mexicanum) Immunology 36 643 648 1:CAS:528:DyaE1MXksFCns7g%3D
11. VG Chinchar 2002 Ranaviruses (family Iridoviridae): emerging cold-blooded killers Archives of Virology 147 447 470 10.1007/s007050200000 1:CAS:528:DC%2BD38Xkt1egu7w%3D (Pubitemid 34179622)
12. MS Christin AD Gendron P Brousseau L Me'Nard DJ Marcogliese D Cyr S Ruby M Fournier 2003 Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection Environmental Toxicology and Chemistry 22 1127 1133 10.1897/1551-5028(2003)022<1127:EOAPOT>2.0.CO;2 1:CAS:528:DC%2BD3sXjtFCms70%3D (Pubitemid 36438194)
13. JP Collins AS Storfer 2003 Global amphibian declines: sorting the hypotheses Diversity and Distributions 9 89 98 10.1046/j.1472-4642.2003.00012.x (Pubitemid 36317427)
14. JP Collins T Halliday 2005 Forecasting changes in amphibian biodiversity: aiming at a moving target Philosophical Transactions of the British Royal Society: B 360 309 314 10.1098/rstb.2004.1588 (Pubitemid 41529627)
15. A Colombo O Federica P Bonfanti 2005 Exposure to the organophosphorus pesticide chlorpyrifos inhibits acetylcholinesterase activity and affects muscular integrity in Xenopus laevis larvae Chemosphere 61 1665 1671 10.1016/j.chemosphere.2005.04.005 1:CAS:528:DC%2BD2MXht1OrsLfO (Pubitemid 41728197)
16. P Daszak L Berger AA Cunningham AD Hyatt DE Green R Speare 1999 Emerging infectious diseases and amphibian population declines Emerging Infectious Disease 5 735 748 10.3201/eid0506.990601 1:STN:280:DC%2BD3c%2FntVChtQ%3D%3D
17. P Daszak AA Cunningham AD Hyatt 2000 Emerging infectious diseases of wildlife- threats to biodiversity and human health Science 287 443 449 10.1126/science.287.5452.443 1:CAS:528:DC%2BD3cXntl2jtw%3D%3D
18. P Daszak AA Cunningham AD Hyatt 2003 Infectious disease and amphibian population declines Diversity and Distributions 9 141 150 10.1046/j.1472-4642. 2003.00016.x (Pubitemid 36317431)
19. F De Castro B Bolker 2005 Mechanisms of disease-induced extinction Ecology Letters 8 117 126 10.1111/j.1461-0248.2004.00693.x (Pubitemid 40172144)
20. SG Diana WJ Resetarits DJ Schaeffer KB Beckmen VR Beasley 2000 Effects of atrazine on amphibian growth and survival in artificial aquatic communities Environmental Toxicology and Chemistry 19 2961 2967 10.1897/1551-5028(2000) 019<2961:EOAOAG>2.0.CO;2 1:CAS:528:DC%2BD3MXjtVemuw%3D%3D
21. D Forson AS Storfer 2006 Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum Ecological Applications 16 2325 2332 10.1890/1051-0761(2006)016[2325:AIRSIT]2.0.CO;2 (Pubitemid 44917589)
22. D Forson AS Storfer 2006 Effects of atrazine and iridovirus infection on survival and life history characteristics in long-toed salamanders, Ambystoma macrodactylum Environmental Toxicology and Chemistry 25 168 173 10.1897/05-260R.1 1:CAS:528:DC%2BD28XpsVSn (Pubitemid 43031215)
23. TB Hayes A Collins M Lee M Mendoza N Noriega AA Stuart A Vonk 2002 Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses Proceedings of the National Academy of Sciences USA 99 5476 5480 10.1073/pnas.082121499 1:CAS:528:DC%2BD38XjtFKlsbc%3D (Pubitemid 34411573)
24. TB Hayes K Haston M Tsui A Hoang C Haeffele A Vonk 2003 Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence Environmental Health Perspectives 111 568 575 1:CAS:528:DC%2BD3sXjtlKrsr4%3D
25. SH Hurlbert MS Mulla JO Keith WE Westlake ME Düsch 1970 Biological effects and persistence of Dursban in freshwater ponds Journal of Economic Entomology 1 43 52
26. JK Jancovich EW Davidson N Parameswaran J Mao VG Chinchar JP Collins BL Jacobs AS Storfer 2005 Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread Molecular Ecology 14 213 224 10.1111/j.1365-294X.2004.02387.x 1:STN:280:DC%2BD2M%2FhvVykuw%3D%3D (Pubitemid 40141489)
27. JK Jancovich EW Davidson JF Morado BL Jacobs JP Collins 1997 Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi Diseases of Aquatic Organisms 31 161 167 10.3354/dao031161
28. TJ Johnson JM Chase KL Dosch RB Hartson JA Gross DJ Larson DR Sutherland SR Carpenter 2007 Aquatic eutrophication promotes pathogenic infection in amphibians Proceedings of the National Academy of Sciences USA 104 15781 15786 10.1073/pnas.0707763104 1:CAS:528:DC%2BD2sXhtFGns7zP (Pubitemid 350035377)
29. Kiely T, Donaldson D, Grude A (2004) Pesticide industry sales and usage: 2000 and 2001 market estimates. EPA(7503C)-733-R-04-001. Final/Technical Report. U.S. Environmental Protection Agency, Washington, DC
30. JM Kiesecker 2002 Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences USA 99 9900 9904 10.1073/pnas.152098899 1:CAS:528:DC%2BD38XlslKgsbw%3D (Pubitemid 34831144)
31. DL Larson S McDonald AJ Fivizzani WE Newton SJ Hamilton 1998 Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: Duration, larval growth, and hormonal response Physiological Zoology 71 671 679 1:CAS:528:DyaK1cXntFSnur8%3D
32. L Manzanti C Rice K Bialek D Sparling C Stevenson WE Johnson P Kangas J Rheinstein 2003 Aqueous-phase disappearance of atrazine, metolachlor, and chlorpyrifos in laboratory aquaria and outdoor macrocosms Archives of Environmental Contamination and Toxicology 44 67 76 10.1007/s00244-002-1259-3 (Pubitemid 36134830)
33. LL McConnell JS LeNoir S Datta JN Seiber 1998 Wet deposition of current-use pesticides in the Sierra Nevada mountain range, California, USA Environmental Toxicology and Chemistry 17 1908 1916 10.1897/1551-5028(1998) 017<1908:WDOCUP>2.3.CO;2 1:CAS:528:DyaK1cXmtlCgsro%3D (Pubitemid 28449620)
34. H McCallum A Dobson 1995 Detecting disease and parasite threats to endangered species and ecosystems Trends in Ecology & Evolution 10 190 194 10.1016/S0169-5347(00)89050-3
35. R Relyea J Hoverman 2006 Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems Ecology Letters 9 1157 1171 10.1111/j.1461-0248.2006.00966.x (Pubitemid 44401587)
36. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008) Agrochemicals increase trematode infections in a declining amphibian species. Nature doi: 10.1038/nature07281
37. JR Rohr T Sager TM Sesterhenn BD Palmer 2006 Exposure, postexposure, and density-mediated effects of atrazine on amphibians: breaking down net effects into their parts Environmental Health Perspectives 114 46 50 1:CAS:528:DC%2BD28XosVOjsw%3D%3D
38. KR Solomon DB Baker RP Richards KR Dixon SJ Klaine TW La Point RJ Kendall CP Weisskopf JM Giddings JP Giesy LW Hall Jr WM Williams 1996 Ecological risk assessment of atrazine in North American surface waters Environmental Toxicology and Chemistry 15 31 76 10.1897/1551-5028(1996)015<0031:ERAOAI>2.3.CO;2 1:CAS:528:DyaK28XhvF2lsQ%3D%3D (Pubitemid 26106920)
39. A Storfer ME Alfaro BJ Ridenhour JK Jancovich SG Mech MJ Parris JP Collins 2007 Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic Ecology Letters 10 1075 1083 10.1111/j.1461-0248.2007.01102.x (Pubitemid 47512354)
40. SI Storrs JM Kiesecker 2004 Survivorship patterns of larval amphibians exposed to low concentrations of atrazine Environmental Health Perspectives 112 1054 1057 1:CAS:528:DC%2BD2cXps1agsLc%3D
41. SN Stuart JS Chanson NA Cox BE Young ASL Rodrigues DL Fischman RW Waller 2004 Status and trends of amphibian declines and extinctions worldwide Science 306 1783 1786 10.1126/science.1103538 1:CAS:528:DC%2BD2cXhtVKitb7E (Pubitemid 39601397)
42. PJ van den Brink RPA van Wijngaarden WGH Lucassen TCM Brock P Leeuwangh 1996 Effects of the insecticide Dursban 4E (active ingredient chlorpyrifos) in outdoor experimental ditches: II. Invertebrate community responses and recovery Environmental Toxicology and Chemistry 15 1133 1142 10.1897/1551-5028(1996) 015<1133:EOTIDA>2.3.CO;2 (Pubitemid 26295021)
43. MN Wacksman JD Maul MJ Lydy 2006 Impact of atrazine on chlorpyrifos toxicity in four aquatic vertebrates Archives of Environmental Contamination and Toxicology 51 681 689 10.1007/s00244-005-0264-8 1:CAS:528:DC%2BD28XhtVOmu7jJ (Pubitemid 44581834)
44. PD Widder JR Bidwell 2006 Cholinesterase activity and behavior in chlorpyrifos-exposed Rana sphenocephala tadpoles Environmental Toxicology and Chemistry 25 2446 2454 10.1897/05-522R.1 1:CAS:528:DC%2BD28XovVOrt7o%3D (Pubitemid 44763302)