Plant-rodent interactions after a heavy snowfall decrease plant regeneration and soil carbon emission in an old-growth forest

Qingqiu Zhou; Debao Li; Shangwen Xia; Zhe Chen; Bo Wang; Jianping Wu

doi:10.1186/s40663-021-00310-2

Forest Ecosystems 2021, 8(2): 30 https://doi.org/10.1186/s40663-021-00310-2

Research |

Open Access | Issue | Published: 17 May 2021

Plant-rodent interactions after a heavy snowfall decrease plant regeneration and soil carbon emission in an old-growth forest

Show Author's Information Hide Author's Information Qingqiu Zhou^{¹^,²}, Debao Li^{¹^,²}, Shangwen Xia^³, Zhe Chen^{¹^,²}, Bo Wang^⁴, Jianping Wu^{¹^,²}

Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology, Yunnan University, Kunming, 650500, China

Key Laboratory of Soil Ecology and Health in Universities of Yunnan Province, School of Ecology and Environmental Sciences, Yunnan University, Kunming, 650500, China

Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, 666303, China

School of Resources and Environmental Engineering, Anhui University, Hefei, 230601, China

Keywords:

Forest ecosystem, Enzyme activity, Climate extreme, PLFAs, Soil respiration

Cite this article:

Zhou Q, Li D, Xia S, et al. Plant-rodent interactions after a heavy snowfall decrease plant regeneration and soil carbon emission in an old-growth forest. Forest Ecosystems, 2021, 8(2): 30. https://doi.org/10.1186/s40663-021-00310-2

Download citation

EndNote(RIS)

BibTeX

273

Views

Downloads

Citations

Crossref

WoS

Scopus

CSCD

Abstract Full text About this article

Abstract

Background

Climate extremes are likely to become more common in the future and are expected to change ecosystem processes and functions. As important consumers of seeds in forests, rodents are likely to affect forest regeneration following an extreme weather event. In April 2015, we began a field experiment after an extreme snowfall event in January 2015 in a primary forest that was > 300 years old. The heavy snow broke many tree limbs, which presumably reduced the numbers of seeds produced. Two treatments (rodent exclusion and rodent access) were established in the forest, in which rodent exclusion were achieved by placing stainlessness nets around the plot borders. Plant abundance, plant species richness, soil properties, soil microbial community composition, basal and substrate-induced respiration were determined in December 2017.

Results

Plant abundance and species richness significantly increased, but soil microbial biomass decreased with rodent exclusion. Urease activity and soil basal respiration also significantly decreased with rodent exclusion. Most other soil properties, however, were unaffected by rodent exclusion. The relative effects of multiple predictors of basal respiration were mainly explained by the composition of the soil microbial community.

Conclusions

After a heavy snowfall in an old-growth forest, exclusion of rodents increased plant regeneration and reduced microbial biomass and soil basal respiration. The main factor associated with the reduction in soil basal respiration was the change in the composition of the soil microbial community. These findings suggest that after a heavy snowfall, rodents may interfere with forest regeneration by directly reducing plant diversity and abundance but may enhance carbon retention by indirectly altering the soil microbial community.

Full text

Abstract

Full text

Outline

About this article

Plant-rodent interactions after a heavy snowfall decrease plant regeneration and soil carbon emission in an old-growth forest

Show Author's information Hide Author's Information Qingqiu Zhou^{¹^,²}, Debao Li^{¹^,²}, Shangwen Xia^³, Zhe Chen^{¹^,²}, Bo Wang^⁴, Jianping Wu^{¹^,²}

Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology, Yunnan University, Kunming, 650500, China

Key Laboratory of Soil Ecology and Health in Universities of Yunnan Province, School of Ecology and Environmental Sciences, Yunnan University, Kunming, 650500, China

Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, 666303, China

School of Resources and Environmental Engineering, Anhui University, Hefei, 230601, China

Abstract

Background

Results

Conclusions

Keywords: Forest ecosystem, Enzyme activity, Climate extreme, PLFAs, Soil respiration

References(47)

Ashley WS, Haberlie AM, Gensini VA (2020) Reduced frequency and size of late-twenty-first-century snowstorms over North America. Nat Clim Chang 10(6): 539-544. https://doi.org/10.1038/s41558-020-0774-4

DOI Google Scholar

Bardgett RD, Caruso T (2020) Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states. Philos Trans R Soc B-Biol Sci 375(1794): 20190112. https://doi.org/10.1098/rstb.2019.0112

DOI Google Scholar

Bardgett RD, Hobbs PJ, Frostegård Å (1996) Changes in soil fungal: bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biol Fertil Soils 22(3): 261-264. https://doi.org/10.1007/BF00382522

DOI Google Scholar

Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528): 505-511. https://doi.org/10.1038/nature13855

DOI Google Scholar

Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84(9): 2258-2268. https://doi.org/10.1890/02-0274

DOI Google Scholar

Boone SR, Mortelliti A (2019) Small mammal tree seed selection in mixed forests of the eastern United States. Forest Ecol Manage 449: 117487. https://doi.org/10.1016/j.foreco.2019.117487

DOI Google Scholar

Cao L, Wang Z, Yan C, Chen J, Guo C, Zhang Z (2016) Differential foraging preferences on seed size by rodents result in higher dispersal success of medium-sized seeds. Ecology 97(11): 3070-3078. https://doi.org/10.1002/ecy.1555

DOI Google Scholar

Contosta AR, Burakowski EA, Varner RK, Frey SD (2016) Winter soil respiration in a humid temperate forest: the roles of moisture, temperature, and snowpack. J Geophys Res-Biogeosci 121(12): 3072-3088. https://doi.org/10.1002/2016JG003450

DOI Google Scholar

Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

Diaz-Yanez O, Mola-Yudego B, Ramon Gonzalez-Olabarria J, Pukkala T (2017) How does forest composition and structure affect the stability against wind and snow? Forest Ecol Manage 401: 215-222. https://doi.org/10.1016/j.foreco.2017.06.054

DOI Google Scholar

Fei SL, Jo I, Guo QF, Wardle DA, Fang JY, Chen AP, Oswalt CM, Brockerhoff EG (2018) Impacts of climate on the biodiversity-productivity relationship in natural forests. Nat Commun 9(1): 5436. https://doi.org/10.1038/s41467-018-07880-w

DOI Google Scholar

Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22(1-2): 59-65. https://doi.org/10.1007/BF00384433

DOI Google Scholar

Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43(8): 1621-1625. https://doi.org/10.1016/j.soilbio.2010.11.021

DOI Google Scholar

Ge J, Xiong G, Wang Z, Zhang M, Zhao C, Shen G, Xu W, Xie Z (2015) Altered dynamics of broad-leaved tree species in a Chinese subtropical montane mixed forest: the role of an anomalous extreme 2008 ice storm episode. Ecol Evol 5(7): 1484-1493. https://doi.org/10.1002/ece3.1433

DOI Google Scholar

Jactel H, Gritti ES, Drossler L, Forrester DI, Mason WL, Morin X, Pretzsch H, Castagneyrol B (2018) Positive biodiversity-productivity relationships in forests: climate matters. Biol Lett 14(4): 20170747. https://doi.org/10.1098/rsbl.2017.0747

DOI Google Scholar

Jing X, Sanders NJ, Shi Y, Chu H, Classen AT, Zhao K (2015) The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat Commun 6(1): 8159. https://doi.org/10.1038/ncomms9159

DOI Google Scholar

Kang H, Chang M, Liu S, Chao Z, Zhang X, Wang D (2020) Rodent-mediated plant community competition: what happens to the seeds after entering the adjacent stands? Forest Ecosyst 7(1): 56. https://doi.org/10.1186/s40663-020-00270-z

DOI Google Scholar

Kayler ZE, De Boeck HJ, Fatichi S, Gruenzweig JM, Merbold L, Beier C, McDowell N, Dukes JS (2015) Experiments to confront the environmental extremes of climate change. Front Ecol Environ 13(4): 219-225. https://doi.org/10.1890/140174

DOI Google Scholar

Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015) Dynamics of global forest area: results from the FAO global forest resources assessment 2015. For Ecol Manag 352: 9-20. https://doi.org/10.1016/j.foreco.2015.06.014

DOI Google Scholar

Lang ZW, Wang B (2016) The effect of seed size on seed fate in a subtropical forest, southwest of China. iForest-Biogeosci For 9: 652-657

DOI Google Scholar

Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vazquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6(1): 6707. https://doi.org/10.1038/ncomms7707

DOI Google Scholar

Lehtonen I, Kamarainen M, Gregow H, Venalainen A, Peltola H (2016) Heavy snow loads in Finnish forests respond regionally asymmetrically to projected climate change. Nat Hazards Earth Syst Sci 16(10): 2259-2271. https://doi.org/10.5194/nhess-16-2259-2016

DOI Google Scholar

Li W, Wu J, Bai E, Jin C, Wang A, Yuan F, Guan D (2016) Response of terrestrial carbon dynamics to snow cover change: a meta-analysis of experimental manipulation (Ⅱ). Soil Biol Biochem 103: 388-393. https://doi.org/10.1016/j.soilbio.2016.09.017

DOI Google Scholar

Liu G (1996) Soil physical and chemical analysis and description of soil profiles. China Standard Press, Beijing (in Chinese)

Luyssaert S, Schulze ED, Börner A, Knohl A, Hessenmöller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455(7210): 213-215. https://doi.org/10.1038/nature07276

DOI Google Scholar

Morales-Hidalgo D, Oswalt SN, Somanathan E (2015) Status and trends in global primary forest, protected areas, and areas designated for conservation of biodiversity from the global forest resources assessment 2015. Forest Ecol Manage 352: 68-77. https://doi.org/10.1016/j.foreco.2015.06.011

DOI Google Scholar

Mundim FM, Bruna EM (2016) Is there a temperate bias in our understanding of how climate change will alter plant-herbivore interactions? A meta-analysis of experimental studies. Am Nat 188(S1): S74-S89. https://doi.org/10.1086/687530

DOI Google Scholar

Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao S, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world's forests. Science 333(6045): 988-993. https://doi.org/10.1126/science.1201609

DOI Google Scholar

Peltola H, Nykanen ML, Kellomaki S (1997) Model computations on the critical combination of snow loading and windspeed for snow damage of scots pine, Norway spruce and birch sp. at stand edge. Forest Ecol Manage 95(3): 229-241. https://doi.org/10.1016/S0378-1127(97)00037-6

DOI Google Scholar

Reyer CPO, Brouwers N, Rammig A, Brook BW, Epila J, Grant RF, Holmgren M, Langerwisch F, Leuzinger S, Lucht W, Medlyn B, Pfeifer M, Steinkamp J, Vanderwel MC, Verbeeck H, Villela DM (2015) Forest resilience and tipping points at different spatio-temporal scales: approaches and challenges. J Ecol 103(1): 5-15. https://doi.org/10.1111/1365-2745.12337

DOI Google Scholar

Sitters J, Venterink HO (2015) The need for a novel integrative theory on feedbacks between herbivores, plants and soil nutrient cycling. Plant Soil 396(1-2): 421-426. https://doi.org/10.1007/s11104-015-2679-y

DOI Google Scholar

Song QH, Fei XH, Zhang YP, Sha LQ, Wu CS, Lu ZY, Luo K, Zhou WJ, Liu YT, Gao JB (2017a) Snow damage strongly reduces the strength of the carbon sink in a primary subtropical evergreen broadleaved forest. Environ Res Lett 12: 104014

DOI Google Scholar

Song X, Hogan JA, Brown C, Cao M, Yang J (2017b) Snow damage to the canopy facilitates alien weed invasion in a subtropical montane primary forest in southwestern China. Forest Ecol Manage 391: 275-281. https://doi.org/10.1016/j.foreco.2017.02.031

DOI Google Scholar

Stephenson NL, Das AJ, Condit R, Russo SE, Baker PJ, Beckman NG, Coomes DA, Lines ER, Morris WK, Rüger N, Álvarez E, Blundo C, Bunyavejchewin S, Chuyong G, Davies SJ, Duque Á, Ewango CN, Flores O, Franklin JF, Grau HR, Hao Z, Harmon ME, Hubbell SP, Kenfack D, Lin Y, Makana JR, Malizia A, Malizia LR, Pabst RJ, Pongpattananurak N, Su SH, Sun IF, Tan S, Thomas D, van Mantgem PJ, Wang X, Wiser SK, Zavala MA (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507(7490): 90-93. https://doi.org/10.1038/nature12914

DOI Google Scholar

Tan ZH, Zhang YP, Schaefer D, Yu GR, Liang N, Song QH (2011) An old-growth subtropical Asian evergreen forest as a large carbon sink. Atmos Environ 45(8): 1548-1554. https://doi.org/10.1016/j.atmosenv.2010.12.041

DOI Google Scholar

Ullah S, Muhammad B, Amin R, Haider AH (2019) Sensitivity of Arbuscular mycorrhizal fungi in old-growth forest: direct effect on growth and soil carbon storage. Appl Ecol Environ Res J 17: 13749-13758

DOI Google Scholar

Venalainen A, Lehtonen I, Laapas M, Ruosteenoja K, Tikkanen OP, Viiri H, Ikonen VP, Peltola H (2020) Climate change induces multiple risks to boreal forests and forestry in Finland: a literature review. Glob Chang Biol 26(8): 4178-4196. https://doi.org/10.1111/gcb.15183

DOI Google Scholar

Wang B, Philips JS, Tomlinson KW (2013) Tradeoff between physical and chemical defense in plant seeds is mediated by seed mass. Oikos 127: 440-447

DOI Google Scholar

Wang B, Philips JS, Tomlinson KW (2013a) Tradeoff between physical and chemical defense in plant seeds is mediated by seed mass. Oikos 127: 440-447

DOI Google Scholar

Wang B, Ye CX, Cannon CH, Chen J (2013b) Dissecting the decision making process of scatter-hoarding rodents. Oikos 122(7): 1027-1034. https://doi.org/10.1111/j.1600-0706.2012.20823.x

DOI Google Scholar

Wardle DA, Zackrisson O (2005) Effects of species and functional group loss on island ecosystem properties. Nature 435(7043): 806-810. https://doi.org/10.1038/nature03611

DOI Google Scholar

Wu J, Liu Z, Chen D, Huang G, Zhou L, Fu S (2011) Understory plants can make substantial contributions to soil respiration: evidence from two subtropical plantations. Soil Biol Biochem 43(11): 2355-2357. https://doi.org/10.1016/j.soilbio.2011.07.011

DOI Google Scholar

Xu J, Xue L, Su Z (2016) Impacts of forest gaps on soil properties after a severe ice storm in a Cunninghamia lanceolata stand. Pedosphere 26(3): 408-416. https://doi.org/10.1016/S1002-0160(15)60053-4

DOI Google Scholar

Yang X, Yan C, Gu H, Zhang Z (2020) Interspecific synchrony of seed rain shapes rodent-mediated indirect seed-seed interactions of sympatric tree species in a subtropical forest. Ecol Lett 23(1): 45-54. https://doi.org/10.1111/ele.13405

DOI Google Scholar

Zhao CY, Fang YH, Luo Y, Wang J (2016) Interdecadal component variation characteristics in heavy winter snow intensity in north-eastern China and its response to sea surface temperatures. Atmos Res 180:165-177. https://doi.org/10.1016/j.atmosres.2016.05.016

DOI Google Scholar

Zhou G, Liu S, Li Z, Zhang D, Tang X, Zhou C, Yan J, Mo J (2006) Old-growth forests can accumulate carbon in soils. Science 314(5804): 1417. https://doi.org/10.1126/science.1130168

DOI Google Scholar

Zhou Y, Newman C, Chen J, Xie Z, Macdonald DW (2013) Anomalous, extreme weather disrupts obligate seed dispersal mutualism: snow in a subtropical forest ecosystem. Glob Chang Biol 19(9): 2867-2877. https://doi.org/10.1111/gcb.12245

DOI Google Scholar

About this article

Publication history

Acknowledgements

Rights and permissions

Publication history

Received: 10 January 2021

Accepted: 27 April 2021

Published: 17 May 2021

Issue date: June 2021

Copyright

Acknowledgements

We thank Zhiyun Lu and Hangdong Wen from the Ailaoshan Station for Subtropical Forest Ecosystem Studies for their field assistance. We also thank three anonymous reviewers for their insightful comments.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.