Abstract
Bark beetle outbreaks are increasing in frequency and intensity, generating massive inventories of dead trees globally. During attacks, trees are pre-inoculated with ophiostomatoid fungi via bark beetles, which has been shown to increase termite presence and feeding. These events may, in turn, alter biogeochemical cycles during decomposition. We examined these relationships by experimentally inoculating dead wood with bluestain fungi in a temperate pine forest. Across ten replicate plots, eight 0.5 m-long logs were inoculated with Ophiostoma minus and eight with distilled water. Half of the logs from each inoculation treatment were covered from above with a mesh cage barrier to exclude aboveground beetles while permitting access by belowground decomposers. After 1 year, significant increases in mass (34%) and decreases in moisture content (− 17%) were observed across all treatments, but no consistent changes in density were evident. C concentrations were 12% greater in bark when barriers were present and 17% greater in sapwood when barriers and inoculation fungi were absent. N concentrations were 16% greater in bark for fungal-inoculated logs and 27% greater when barriers were present. C:N ratios in A horizon soils under fungal-inoculated logs were 12% greater. Furthermore, termites were present fourfold more in fungal-inoculated logs than controls and the presence of termites was associated with 6% less C in sapwood and 11% more N in both sapwood and heartwood. Together these results suggest dead wood generated via bark beetle attacks has different biogeochemical responses during initial decomposition phases, which could have implications for the C status in forests following bark beetle outbreaks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amburgey T (1979) Review and checklist of the literature on interactions between wood-inhabiting fungi and subterranean termites. 1960–1978. Sociobiology 4:279–296
André F, Jonard M, Ponette Q (2008) Spatial and temporal patterns of throughfall chemistry within a temperate mixed oak–beech stand. Sci Total Environ 397:215–228. https://doi.org/10.1016/j.scitotenv.2008.02.043
Ballard RG, Walsh MA, Cole WE (1984) The penetration and growth of blue-stain fungi in the sapwood of lodgepole pine attacked by mountain pine beetle. Can J Bot 62:1724–1729. https://doi.org/10.1139/b84-233
Bearup LA, Maxwell RM, Clow DW, McCray JE (2014) Hydrological effects of forest transpiration loss in bark beetle-impacted watersheds. Nat Clim Chang 4:481–486. https://doi.org/10.1038/nclimate2198
Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:1377–1383. https://doi.org/10.1139/b95-400
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. https://doi.org/10.1126/science.1155121
Bradford MA, Warren RJ II, Baldrian P et al (2014) Climate fails to predict wood decomposition at regional scales. Nat Clim Chang 4:625–630
Bright D (2014) A catalog of Scolytidae and Platypodidae (Coleoptera), Supplement 3(2000–2010). NRC Research Press, Ottawa
Brouillard BM, Mikkelson KM, Bokman CM et al (2017) Extent of localized tree mortality influences soil biogeochemical response in a beetle-infested coniferous forest. Soil Biol Biochem 114:309–318. https://doi.org/10.1016/j.soilbio.2017.06.016
Busse MD (1994) Downed bole-wood decomposition in lodgepole pine forests of central Oregon. Soil Sci Soc Am J 58:221. https://doi.org/10.2136/sssaj1994.03615995005800010033x
Buttle JM, Toye HJ, Greenwood WJ, Bialkowski R (2014) Stemflow and soil water recharge during rainfall in a red pine chronosequence on the Oak Ridges Moraine, southern Ontario, Canada. J Hydrol 517:777–790. https://doi.org/10.1016/J.JHYDROL.2014.06.014
Carpenter SE, Harmon ME, Ingham ER et al (1988) Early patterns of heterotroph activity in conifer logs. In: Boddy L, Lyon A, Watling R (eds) Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences. Royal Society of Edinburgh Scotland Foundation, London, pp 33–43
Chambers JQ, Higuchi N, Schimel JP et al (2000) Decomposition and carbon cycling of dead trees in tropical forests of the central Amazon. Oecologia 122:380–388. https://doi.org/10.1007/s004420050044
Chambers JQ, Schimel JP, Nobre AD (2001) Respiration from coarse wood litter in central Amazon forests. Biogeochemistry 52:115–131. https://doi.org/10.1023/A:1006473530673
Chen Y, Forschler BT (2016) Elemental concentrations in the frass of saproxylic insects suggest a role in micronutrient cycling. Ecosphere 7:e01300. https://doi.org/10.1002/ecs2.1300
Chouvenc T, Su N-Y (2010) Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events: limits and potential for biological control. J Econ Entomol 103:1327–1337. https://doi.org/10.1603/EC09407
Clay NA, Little N, Riggins JJ (2017) Inoculation of ophiostomatoid fungi in loblolly pine trees increases the presence of subterranean termites in fungal lesions. Arthropod Plant Interact 11:213–219. https://doi.org/10.1007/s11829-016-9473-5
Coulson RN, Klepzig K (2011) Southern Pine Beetle II. Gen Tech Rep SRS-140 Asheville, NC US Dep Agric For Serv South Res Station 512 p 140:1–512
Edmonds RL, Eglitis A (1989) The role of the Douglas-fir beetle and wood borers in the decomposition of and nutrient release from Douglas-fir logs. Can J For Res 19:853–859. https://doi.org/10.1139/x89-130
Fan J, Oestergaard KT, Guyot A et al (2015) Spatial variability of throughfall and stemflow in an exotic pine plantation of subtropical coastal Australia. Hydrol Process 29:793–804. https://doi.org/10.1002/hyp.10193
Forrester JA, Mladenoff DJ, D’Amato AW et al (2015) Temporal trends and sources of variation in carbon flux from coarse woody debris in experimental forest canopy openings. Oecologia 179:889–900. https://doi.org/10.1007/s00442-015-3393-4
Goodale CL, Apps MJ, Birdsey RA et al (2002) Forest carbon sinks in the northern hemisphere. Ecol Appl 12:891–899. https://doi.org/10.1890/1051-0761(2002)012%5b0891:FCSITN%5d2.0.CO;2
Gough CM, Vogel CS, Kazanski C et al (2007) Coarse woody debris and the carbon balance of a north temperate forest. For Ecol Manag 244:60–67. https://doi.org/10.1016/j.foreco.2007.03.039
Goulden ML, McMillan AMS, Wintston GC et al (2011) Patterns of NPP, GPP, respiration, and NEP during boreal forest succession. Glob Chang Biol 17:855–871. https://doi.org/10.1111/j.1365-2486.2010.02274.x
Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu Rev Ecol Syst 33:1–23. https://doi.org/10.1146/annurev.ecolsys.33.010802.150507
Hafner SD, Groffman PM (2005) Soil nitrogen cycling under litter and coarse woody debris in a mixed forest in New York State
Hanula JL (1996) Relationship of wood-feeding insects and coarse woody debris. In: McMinn J (ed) Proceedings of the workshop on coarse woody debris in southern forests: effects on biodiversity. United States Department of Agriculture, Athens, pp 55–81
Harmon ME (2009) Woody detritus its contribution to carbon dynamics of old-growth forests: the temporal context. In: Wirth C, Gleixner G, Heimann M (eds) Old growth forests. Springer, Berlin, pp 159–190
Harmon ME, Franklin JF, Swanson FJ, et al (1986) Ecology of coarse woody debris in temperate ecosystems, pp 133–302
Harmon ME, Krankina ON, Sexton J (2011) Decomposition vectors: a new approach to estimating woody detritus decomposition dynamics. Can J For Res 30:76–84
Hicke JA, Allen CD, Desai AR et al (2012) Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Glob Change Biol 18:7–34. https://doi.org/10.1111/j.1365-2486.2011.02543.x
Holub SM, Spears JD, Lajtha K (2001) A reanalysis of nutrient dynamics in coniferous coarse woody debris. Can J For Res 31:1894–1902. https://doi.org/10.1139/x01-125
Huber C, Baumgarten M, Göttlein A, Rotter V (2004) Nitrogen turnover and nitrate leaching after bark beetle attack in mountainous spruce stands of the Bavarian Forest National Park. Water Air Soil Pollut Focus 4:391–414. https://doi.org/10.1023/B:WAFO.0000028367.69158.8d
Johnson CE, Siccama TG, Denny EG et al (2014) In situ decomposition of northern hardwood tree boles: decay rates and nutrient dynamics in wood and bark. Can J For Res 44:1515–1524. https://doi.org/10.1139/cjfr-2014-0221
Jouquet P, Traoré S, Choosai C et al (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur J Soil Biol 47:215–222. https://doi.org/10.1016/J.EJSOBI.2011.05.005
Keith H, Wong S (2006) Measurement of soil CO2 efflux using soda lime absorption: both quantitative and reliable. Soil Biol Biochem 38:1121–1131. https://doi.org/10.1016/j.soilbio.2005.09.012
Kurz WA, Dymond CC, Stinson G et al (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990. https://doi.org/10.1038/nature06777
Laiho R, Prescott CE (2004) Decay and nutrient dynamics of coarse woody debris in northern coniferous forests: a synthesis. Can J For Res 34:763–777. https://doi.org/10.1139/x03-241
Le Mellec A, Meesenburg H, Michalzik B (2010) The importance of canopy-derived dissolved and particulate organic matter (DOM and POM)—comparing throughfall solution from broadleaved and coniferous forests. Ann For Sci 67:411. https://doi.org/10.1051/forest/2009130
Levia DF, Frost EE (2006) Variability of throughfall volume and solute inputs in wooded ecosystems. Prog Phys Geogr 30:605–632. https://doi.org/10.1177/0309133306071145
Little NS, Blount NA, Londo AJ et al (2012a) Preference of formosan subterranean termites for blue-stained southern yellow pine sapwood. J Econ Entomol 105:1640–1644. https://doi.org/10.1603/EC12081
Little NS, Riggins JJ, Schultz TP et al (2012b) Feeding preference of native subterranean termites (Isoptera: Rhinotermitidae: Reticulitermes) for wood containing bark beetle pheromones and blue-stain fungi. J Insect Behav 25:197–206. https://doi.org/10.1007/s10905-011-9293-5
Little NS, Schultz TP, Diehl SV et al (2013) Field evaluations of subterranean termite preference for sap-stain inoculated wood. J Insect Behav 26:649–659. https://doi.org/10.1007/s10905-013-9380-x
Liu WH, Bryant DM, Hutyra LR et al (2006) Woody debris contribution to the carbon budget of selectively logged and maturing mid-latitude forests. Oecologia 148:108–117. https://doi.org/10.1007/s00442-006-0356-9
Lovett GM, Lindberg SE (1984) Dry deposition and canopy exchange in a mixed oak forest as determined by analysis of throughfall. J Appl Ecol 21:1013–1027
Magill AH, Aber JD (2000) Variation in soil net mineralization rates with dissolved organic carbon additions. Soil Biol Biochem 32:597–601. https://doi.org/10.1016/S0038-0717(99)00186-8
Mäkipää R, Rajala T, Schigel D et al (2017) Interactions between soil- and dead wood-inhabiting fungal communities during the decay of Norway spruce logs. ISME J 11:1964–1974. https://doi.org/10.1038/ismej.2017.57
Maynard DS, Crowther TW, King JR et al (2015) Temperate forest termites: ecology, biogeography, and ecosystem impacts. Ecol Entomol 40:199–210. https://doi.org/10.1111/een.12185
Moore LD, Van Stan JT, Gay TE et al (2016) Alteration of soil chitinolytic bacterial and ammonia oxidizing archaeal community diversity by rainwater redistribution in an epiphyte-laden Quercus virginiana canopy. Soil Biol Biochem 100:33–41. https://doi.org/10.1016/j.soilbio.2016.05.016
Morehouse K, Johns T, Kaye J, Kaye M (2008) Carbon and nitrogen cycling immediately following bark beetle outbreaks in southwestern ponderosa pine forests. For Ecol Manag 255:2698–2708. https://doi.org/10.1016/j.foreco.2008.01.050
National Oceanic and Atmospheric Administration (2010) National Centers for Environmental Information 1987–2010 US Climate Normals. National Oceanic and Atmospheric Administration, Silver Spring
Natural Resources Conservation Service (2015) Web soil survey. Natural Resources Conservation Service, Washington
Oksanen J, Kindt R, Legendre P, O’Hara RB (2005) Vegan: community ecology package
Pan Y, Birdsey RA, Fang J et al (2011) A large and persistent carbon sink in the world’s forests. Science 80(333):988–993
Progar RA, Schowalter TD, Freitag CM, Morrell JJ (2000) Respiration from coarse woody debris as affected by moisture and saprotroph functional diversity in Western Oregon. Oecologia 124:426–431. https://doi.org/10.1007/PL00008868
Pryor SC, Barthelmie RJ (2005) Liquid and chemical fluxes in precipitation, throughfall, and stemflow: observations from a deciduous forest and a red pine plantation in the midwestern USA. Water Resour Res 163:203–227
R Development Core Team (2007) R: a language and environment for statistical computing. R Development Core Team, Vienna
Riggins JJ, Little NS, Eckhardt LG (2014) Correlation between infection by ophiostomatoid fungi and the presence of subterranean termites in loblolly pine (Pinus taeda L.) roots. Agric For Entomol 16:260–264. https://doi.org/10.1111/afe.12053
Robinson RC (1962) Blue stain fungi in lodgepole pine (Pinus contorta Dougl. var. latifolia engelm.) infested by the mountain pine beetle (Dendroctonus monticolae hopk.). Can J Bot 40:609–614. https://doi.org/10.1139/b62-056
Rosengaus RB, Guldin MR, Traniello JFA (1998) Inhibitory effect of termite fecal pellets on fungal spore germination. J Chem Ecol 24:1697–1706. https://doi.org/10.1023/A:1020872729671
Schowalter T, Caldwell B, Carpenter S et al (1992a) Decomposition of fallen trees: effects of initial conditions and heterotroph colonization rates. In: Singh K (ed) Tropical ecosystems: ecology and management. Wiley Eastern, New Delhi, pp 371–381
Schowalter T, Caldwell B, Carpenter S et al (1992b) Decomposition of fallen trees: effects of initial conditions and heterotroph colonization rates. In: Singh K, Singh J (eds) Tropical ecosystems: ecology and management. Wiley Eastern Limited, New Delhi, pp 373–383
Siegert CM, Levia DF, Hudson SA et al (2016) Small-scale topographic variability influences tree species distribution and canopy throughfall partitioning in a temperate deciduous forest. For Ecol Manag 359:14. https://doi.org/10.1016/j.foreco.2015.09.028
Siegert CM, Levia DF, Leathers DJ et al (2017a) Do storm synoptic patterns affect biogeochemical fluxes from temperate deciduous forest canopies? Biogeochemistry 132:273–292. https://doi.org/10.1007/s10533-017-0300-6
Siegert CM, Renninger HJ, Karunarathna AA, et al (2017b) Biogeochemical hotspots around bark-beetle killed trees. In: Proceedings of the 19th Biennial Southern Silvicultural Research Conference. Blacksburg, VA (in Press)
Silva IC, Rodriguez HG (2001) Interception loss, throughfall and stemflow chemistry in pine and oak forests in northeastern Mexico. Tree Physiol 21:1009–1013. https://doi.org/10.1093/treephys/21.12-13.1009
Smyth CE, Titus B, Trofymow JA et al (2016) Patterns of carbon, nitrogen and phosphorus dynamics in decomposing wood blocks in Canadian forests. Plant Soil 409:459–477. https://doi.org/10.1007/s11104-016-2972-4
Sollins P, Cline SP, Verhoeven T et al (1987) Patterns of log decay in old-growth Douglas-fir forests. Can J For Res 17:1585–1595. https://doi.org/10.1139/x87-243
Spears JD, Holub SM, Harmon ME, Lajtha K (2003) The influence of decomposing logs on soil biology and nutrient cycling in an old-growth mixed coniferous forest in Oregon, USA. Can J For Res 33:2193–2201. https://doi.org/10.1139/x03-148
Sugimoto A, Bignell DE, MacDonald JA (2000) Global impact of termites on the carbon cycle and atmospheric trace gases. Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 409–435
Swift M, Boddy L (1984) Animal–microbial interactions in wood decomposition. In: Anderson J, Rayner A, Walton D (eds) Invertebrate–microbial interactions. Cambridge University Press, Cambridge, pp 89–131
Tang J, Bolstad PV, Desai AR et al (2008) Ecosystem respiration and its components in an old-growth forest in the Great Lakes region of the United States. Agric For Meteorol 148:171–185. https://doi.org/10.1016/j.agrformet.2007.08.008
Ulyshen MD (2015) Insect-mediated nitrogen dynamics in decomposing wood. Ecol Entomol 40:97–112. https://doi.org/10.1111/een.12176
Ulyshen MD, Wagner TL (2013) Quantifying arthropod contributions to wood decay. Methods Ecol Evol 4:345–352. https://doi.org/10.1111/2041-210x.12012
Ulyshen MD, Wagner TL, Mulrooney JE (2014) Contrasting effects of insect exclusion on wood loss in a temperate forest. Ecosphere 5:1–15. https://doi.org/10.1890/ES13-00365.1
Ulyshen MD, Shefferson R, Horn S et al (2017) Below- and above-ground effects of deadwood and termites in plantation forests. Ecosphere 8:e01910. https://doi.org/10.1002/ecs2.1910
Valentini R, Matteucci G, Dolman AJ et al (2000) Respiration as the main determinant of carbon balance in European forests. Nature 404:861–865. https://doi.org/10.1038/35009084
Van Stan JT, Levia DF, Inamdar SP et al (2012) The effects of phenoseason and storm characteristics on throughfall solute washoff and leaching dynamics from a temperate deciduous forest canopy. Sci Total Environ 430:48–58. https://doi.org/10.1016/j.scitotenv.2012.04.060
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton
Wingfield M, Seifert K, Webber J (1993) Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity. American Phytopathological Society Press, St. Paul
Zeng H, Chambers JQ, Negrón-Juárez RI et al (2009) Impacts of tropical cyclones on US forest tree mortality and carbon flux from 1851 to 2000. Proc Natl Acad Sci USA 106:7888–7892. https://doi.org/10.1073/pnas.0808914106
Acknowledgements
This work is a contribution of the Forest and Wildlife Research Center and the Mississippi Agricultural and Forestry Experiment Station, Mississippi State University. This work was funded through the National Science Foundation (DEB # 1660346) and supported by the National Institution of Food and Agriculture, US Department of Agriculture, Mclntire Stennis capacity Grant # MISZ-069390 and Hatch project #069410. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the US Department of Agriculture. This project was made possible by the Mississippi State University Undergraduate Research Scholars Program, the Mississippi Agricultural and Forestry Experiment Station Small Research Initiative program, the Office of Research and Economic Development Cross-College Research Grant, the Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, the Institute for Genomics, Biocomputing and Biotechnology, and the field and laboratory assistance of Craig Bell, Sasith Karunarathna, Katy Limpert, Leana Rapp, Mercedes Siegle-Gaither, Jacob Landfield, John Formby, John Thomason, and Natalie Dearing. Special thanks to Misty Booth and the College of Forest Resources at Mississippi State University for site use in the John W. Starr Experimental Forest. Thank you to anonymous reviewers for their time and careful consideration.
Author information
Authors and Affiliations
Contributions
CMS, NAC, JDT, and JJR conceived and designed the experiments. CMS, NAC, JDT, LGG, and JJR conducted fieldwork. CMS and LGG analyzed the hydrology and soil chemistry data. NAC analyzed the decomposition and invertebrate data. CMS, NAC, JDT, LGG, and JJR wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
J. J. Riggins is an inventor on a patent involving bluestain fungi in baiting methods for termites (US9924706B2). The author and his institution may financially benefit from this patent.
Additional information
Communicated by Hakan Wallander.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Siegert, C.M., Clay, N.A., Tang, J.D. et al. Indirect effects of bark beetle-generated dead wood on biogeochemical and decomposition processes in a pine forest. Oecologia 188, 1209–1226 (2018). https://doi.org/10.1007/s00442-018-4283-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4283-3