Belowground herbivory in red pine stands initiates a cascade that increases abundance of Lyme disease vectors

Forest Ecology and Management

Volumn 302, Issue , 2013, Pages 354-362

  Coyle, David R ^a   Murphy, Matthew W ^b   Paskewitz, Susan M ^a   Orrock, John L ^a   Lee, Xia ^a   Murphy, Robert J ^a,c   McGeehin, Michael A ^b,d   Raffa, Kenneth F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NATIONAL CENTER FOR ENVIRONMENTAL HEALTH   (United States)

^c WISCONSIN DEPARTMENT OF NATURAL RESOURCES   (United States)

^d RTI INTERNATIONAL   (United States)

Author keywords

Borrelia burgdorferi; Environmental precursor; Human disease; Pinus resinosa; Red pine pocket decline; Root herbivory

Indexed keywords

BORRELIA BURGDORFERI; ENVIRONMENTAL PRECURSOR; HERBIVORY; HUMAN DISEASE; PINUS RESINOSA; RED PINES;

FORESTRY;

ECOLOGY;

ABUNDANCE; CONIFEROUS FOREST; DISEASE VECTOR; HERBIVORY; INFECTIOUS DISEASE; LYME DISEASE; MANAGEMENT PRACTICE; PARASITE INFESTATION; PLANTATION; TICK;

DISEASES; ECOLOGY; FORESTRY; PINUS RESINOSA; ROOTS;

GREAT LAKES [NORTH AMERICA]; UNITED STATES; WISCONSIN;

BORRELIA BURGDORFERI; HEXAPODA; IXODES SCAPULARIS; IXODIDA; MAMMALIA; PINUS RESINOSA;

EID: 84877041096     PISSN: 03781127     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foreco.2013.03.017     Document Type: Article

References (47)

1. Allan B.F., Dutra H.P., Goessling L.S., Barnett K., Chase J.M., Marquis R.J., Pang G., Storch G.A., Thach R.E., Orrock J.L. Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proc. Natl. Acad. Sci. USA 2010, 107:18523-18527.
2. Aukema B.H., Zhu J., Møller J., Rasmussen J.G., Raffa K.F. Predisposition to bark beetle attack by root herbivores and associated pathogens: roles in forest decline, gap formation, and persistence of endemic bark beetle populations. Forest Ecol. Manage. 2010, 259:374-382.
3. Caporale D.A., Kocher T.D. Sequence variation in the outer-surface-protein genes of Borrelia burgdorferi. Mol. Biol. Evol. 1994, 11:51-64.
4. Caporale D.A., Johnson C.M., Millard B.J. Presence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) in Southern Kettle Moraine State Forest, Wisconsin, and Characterization of Strain W97F51. J. Med. Entomol. 2005, 42:457-472.
5. Civitello D.J., Flory S.L., Clay K. Exotic grass invasion reduces survival of Ambylomma americanum and Dermacentor variabilis ticks (Acari: Ixodidae). J. Med. Entomol. 2008, 45:867-872.
6. Costa A., Min A., Boone C.K., Kendrick A.P., Murphy R.J., Sharpee W.C., Raffa K.F., Reeve J.D. Dispersal and edge behaviour of bark beetles and predators inhabiting red pine plantations. Agric. Forest Entomol. 2013, 15:1-11.
7. Côté S.D., Rooney T.P., Tremblay J.-P., Dussault C., Waller D.M. Ecological impacts of deer overabundance. Annu. Rev. Ecol. Syst. 2004, 35:113-147.
8. Diuk-Wasser M.A., Gatewood A.G., Cortinas M.R., Yaremych-Hamer S., Tsao J., Kitron U., Hickling G., Brownstein J.S., Walker E., Piesman J., Fish D. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J. Med. Entomol. 2006, 43:166-176.
9. Diuk-Wasser M.A., Vourc'h G., Cislo P., Hoen A.G., Melton F., Rowland M., Cortinas R., Hickling G.J., Tsao J.I., Barbour A.G., Kitron U., Piesman J., Fish D. Field and climate based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Global Ecol. Biogeogr. 2010, 19:504-514.
10. Erbilgin N., Raffa K.F. Spatial analysis of forest gaps resulting from bark beetle colonization of red pines experiencing belowground herbivory and infection. Forest Ecol. Manage. 2003, 177:145-153.
11. Estrada-Peña A. Increasing habitat suitability in the United States for the tick that transmits Lyme disease: a remote sensing approach. Environ. Health Perspect. 2002, 110:635-640.
12. Frank D.H., Fish D., Moy F.H. Landscape features associated with Lyme disease risk in a suburban residential environment. Landsc. Ecol. 1998, 13:27-36.
13. Gerrand A., Keenan R.J., Kanowski P., Stanton R. Australian forest plantations: an overview of industry, environmental, and community issues and benefits. Aust. Forest 2003, 66:1-8.
14. Iverson L.R., Prasad A.M., Matthews S.N., Peters M. Estimating potential habitat for 134 eastern US tree species under six climate scenarios. Forest Ecol. Manage. 2008, 254:390-406.
15. Jactel H., Goulard M., Menassieu P., Goujon G. Habitat diversity in forest plantations reduces infestations of the pine stem borer Dioryctria sylvestrella. J. Appl. Ecol. 2002, 39:618-628.
16. Jakel A., Roth M. Conversion of single-layered Scots pine monocultures into close-to-nature mixed hardwood forests: effects on parasitoid wasps as antagonists. Eur. J. Forest Res. 2004, 123:203-212.
17. Jones C.G., Ostfeld R.S., Richard M.P., Schauber E.M., Wolff J.O. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 1998, 279:1023-1026.
18. Keirans J.E., Hutchinson H.J., Durden L.A., Klompen J.S.H. Ixodes (Ixodes) scapularis (Acari: Ixodidae): rediscription of all active stages, distribution, hosts, geographical variation, and medical and veterinary importance. J. Med. Entomol. 1996, 33:297-318.
19. Klepzig K.D., Raffa K.F., Smalley E.B. Association of an insect-fungal complex with red pine decline in Wisconsin. Forest Sci. 1991, 37:1119-1139.
20. Klepzig K.D., Smalley E.B., Raffa K.F. Dendroctonus valens and Hylastes porculus (Coleoptera: Scolytidae) vectors of pathogenic fungi (Ophiostomatales) associated with Red Pine decline disease. Great Lakes Entomol. 1995, 28:81-87.
21. Klepzig K.D., Smalley E.B., Raffa K.F. Combined chemical defenses against an insect-fungal complex. J. Chem. Ecol. 1996, 22:1367-1388.
22. Koteen L. Climate change, whitebark pine, and grizzly bears in the greater Yellowstone ecosystem. Wildlife Responses to Climate Change: North American Case Studies 2002, 343-414. Island Press, Washington, D.C. S.H. Schneider, T.L. Root (Eds.).
23. Lehmer E.M., Korb J., Bombaci S., McLean N., Ghachu J., Hart L., Kelly A., Jara-Molinar E., O'Brien C., Wright K. The interplay of plant and animal disease in a changing landscape: the role of sudden aspen decline in moderating Sin Nombre virus prevalence in natural deer mouse populations. EcoHealth 2012, 9:205-216.
24. Littell R.C., Milliken G.A., Stroup W.W., Wolfinger R.D., Schabenberger O. SAS System for Mixed Models 2006, SAS Institute, Inc., Cary, NC. 2nd ed.
25. Little, E.L., 1971. Atlas of United States Trees, vol 1, Conifers and Important Hardwoods. U.S. Department of Agriculture Miscellaneous Publication 1146. Washington, D.C., 9 p. + 200 maps.
26. Logan J.A., Macfarlane W.W., Willcox L. Whitebark pine vulnerability to climate-driven mountain pine beetle disturbance in the Greater Yellowstone Ecosystem. Ecol. Appl. 2010, 20:895-902.
27. Manangan J.S., Schweitzer S.H., Nibbelink N., Yabsley M.J., Gibbs S.E., Wimberely M.C. Habitat factors influencing distributions of Anaplasma phagocytophilum and Ehrlichia chaffeensis in the Mississippi alluvial valley. Vector Borne Zoonotic Dis. 2007, 7:563-573.
28. Massung R.F., Slater K., Owens J.H., Nicholson W.L., Mather T.N., Solberg V.B., Olson J.G. Nested PCR assay for detection of granulocytic ehrlichiae. J. Clin. Microbiol. 1998, 36:1090-1095.
29. Masters G.J., Brown V.K., Gange A.C. Plant mediated interactions between above- and below-ground insect herbivores. Oikos 1993, 66:148-151.
30. Otrosina W.J., Bannwart D., Roncadori R.W. Root-infecting fungi associated with a decline of longleaf pine in the southeastern United States. Plant Soil 1999, 217:145-150.
31. Peters D.P.C., Pielke R.A., Bestelmeyer B.T., Allen C.D., Munson-McGee S., Havstad K.M. Cross-scale interactions, nonlinearities, and forecasting catastrophic events. Proc. Natl. Acad. Sci. USA 2004, 101:15130-15135.
32. Prasad, A.M., Iverson, L.R., Matthews, S., Peters, M., 2007-ongoing. A Climate Change Atlas for 134 Forest Tree Species of the Eastern United States [database]. <, Northern Research Station, USDA Forest Service, Delaware, Ohio. http://www.nrs.fs.fed.us/atlas/tree>.
33. Raffa K.F., Aukema B.H., Bentz B.J., Carroll A.L., Hicke J.A., Turner M.G., Romme W.H. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 2008, 58:501-517.
34. Rieske L.K., Raffa K.F. Dispersal patterns and mark-and-recapture estimates of two pine root weevil species, Hylobius pales and Pacylobius picivorus (Coleoptera: Curculionidae), in Christmas tree plantations. Environ. Entomol. 1990, 19:1829-1836.
35. Ryall K.L., Fahrig L. Habitat loss decreases predator-prey ratios in a pine-bark beetle system. Oikos 2005, 110:265-270.
36. Scheller R.M., Mladenoff D.J. A spatially dynamic simulation of the effects of climate change, harvesting, wind, and tree species migration on the forest composition, and biomass in northern Wisconsin, USA. Global Change Biol. 2005, 11:307-321.
37. Steiner F.E., Pinger R.R., Vann C.N., Abley M.J., Sullivan B., Grindle N., Clay K., Fuqua C. Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari; Ixodidae) collected in Indiana. J. Med. Entomol. 2006, 43:437-442.
38. Swei A., Ostfeld R.S., Lane R.S., Briggs C.J. Effects of an invasive forest pathogen on abundance of ticks and their vertebrate hosts in a California Lyme disease focus. Oecologia 2011, 166:91-100.
39. Swei A., Briggs C.J., Lane R.S., Ostfeld R.S. Impacts of an introduced forest pathogen on the risk of Lyme disease in California. Vector Borne Zoonotic Dis. 2012, 8:623-632.
40. Townsend P.A., Eshleman K.N., Welcker C. Remote sensing of gypsy moth defoliation to assess variations in stream nitrogen concentrations. Ecol. Appl. 2004, 14:504-516.
41. Vittor A.Y., Pan W., Gilman R.H., Tielsch J., Glass G., Shields T., Sanchez- Lozano W., Pinedo V.V., Salas-Cobos E., Flores S., Patz J.A. Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am. J. Trop. Med. Hyg. 2009, 81:5-12.
42. Williams S.C., Ward J.S. Effects of Japanese barberry (Ranunculales: Berberidaceae) removal and resulting microclimate changes on Ixodes scapularis (Acari: Ixodidae) abundances in Connecticut, USA. Environ. Entomol. 2010, 39:1911-1921.
43. Williams S.C., Ward J.S., Worthley T.E., Stafford K.C. Managing Japanese Barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environ. Entomol. 2009, 38:977-984.
44. Wilson, L.F., Millers, I., 1982. Pine Root Collar Weevil - Its Ecology and Management. Tech. Bull 1675. U.S. Department of Agriculture, Washington, D.C.
45. van der Putten W.H., Bardgett R.D., de Ruiter P.C., Hol W.H.G., Meyer K.M., Bezemer T.M., Bradford M.A., Christensen S., Eppinga M.B., Fukami T., Hemerik L., Molofsky J., Schadler M., Scherber C., Strauss S.Y., Vos M., Wardle D.A. Emperical and theoretical challenges in aboveground-belowground ecology. Oecologia 2009, 161:1-14.
46. Yuval B., Spielman A. Duration and regulation of the developmental cycle of Ixodes dammini (Acari: Ixodidae). J. Med. Entomol. 1990, 27:196-201.
47. Zhu J., Rasmussen J.G., Moller J.M., Aukema B.H., Raffa K.F. Spatial-temporal modeling of forest gaps generated by colonization from below- and above-ground bark beetle species. J. Am. Stat. Assoc. 2008, 103:162-177.