Plant competition and insect herbivory mediate the impact of invasive plants on soil bacterial community and function

Dong Qing-Qing; Zhang Kao-Ping; He Min-Yan; Huang Wei

doi:10.11913/PSJ.2095-0837.2022.20155

Plant Science Journal > 2022 > 40(2): 155-168. > DOI: 10.11913/PSJ.2095-0837.2022.20155 CSTR: 32231.14.PSJ.2095-0837.2022.20155

Dong Qing-Qing, Zhang Kao-Ping, He Min-Yan, Huang Wei. Plant competition and insect herbivory mediate the impact of invasive plants on soil bacterial community and function[J]. Plant Science Journal, 2022, 40(2): 155-168. DOI: 10.11913/PSJ.2095-0837.2022.20155

Citation:

PDF (1646 KB)

Plant competition and insect herbivory mediate the impact of invasive plants on soil bacterial community and function

Dong Qing-Qing^1,2,3,4,
Zhang Kao-Ping^3,5,
He Min-Yan^3,5, ,,
Huang Wei^3,5, ,

1. Research Center for Ecology and Environment of Qinghai-Tibetan Plateau, Tibet University, Lhasa 850000, China;
2. College of Science, Tibet University, Lhasa 850000, China;
3. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China;
4. University of Chinese Academy of Sciences, Beijing 100049, China;
5. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan 430074, China

Funds:

This work was supported by grants from the National Natural Science Foundation of China (31822007, 32071660, 31870364).

More Information

Received Date: January 06, 2022
Revised Date: January 19, 2022
Available Online: October 31, 2022
Published Date: April 27, 2022

Graphical Abstract

Abstract

Abstract

Exotic plant invasion is an important driver of biodiversity loss. However, little is known regarding how exotic species influence biodiversity belowground and whether such impact can be regulated by other biotic stresses, such as plant competition and insect herbivory. In this study, we used the invasive plant Alternanthera philoxeroides (Mart.) Griseb, native congener Alternanthera sessilis (L.) DC, biocontrol agent Agasicles hygrophila (Selman & Vogt), and native insect Cassida piperata (Coleoptera:Cassididae) as a study system. We established three plant combinations (monoculture of Alternanthera philoxeroides, monoculture of Alternanthera sessilis, and mixture of Alternanthera philoxeroides and Alternanthera sessilis) and four insect herbivory treatments (no insect herbivory, Agasicles hygrophila herbivory, C. piperata herbivory, and Agasicles hygrophila + C. piperata herbivory). We examined how plant competition and insect herbivory mediates the impact of invasive plants on soil bacterial community using high throughput sequencing. We found that plant competition, herbivory treatment, and their interaction did not affect the observed sub-operational taxonomic unit (OTU), Shannon, Phylogenetic diversity, and Evenness indices. These results indicated that neither Alternanthera philoxeroides nor Alternanthera sessilis affected alpha diversity of soil bacteria, and plant competition and herbivory did not exert a mediating effect. In contrast, plant competition strongly affected the composition and structure of the soil bacterial community, decreasing the relative abundance of Chlorobacteria and chemoheterotrophic bacteria while increasing the relative abundance of Acidobacteria. Moreover, plant competition and its interaction with herbivory further regulated the impact of Alternanthera philoxeroides on soil bacterial community composition and structure as well as dominant and functional phyla. Our study indicated that such impact was further regulated by other biotic stresses. Therefore, biotic factors should be included when evaluating the impact of invasive species on biodiversity.
- Invasive plant,
- Plant competition,
- Insect herbivory,
- Soil bacteria community and structure,
- Alpha diversity

FullText(HTML)

References (51)

References

[1]	Livingstone SW, Isaac ME, Cadotte MW. Invasive dominance and resident diversity:unpacking the impact of plant invasion on biodiversity and ecosystem function[J]. Ecol Monogr, 2020, 90(4):e01425.
[2]	Schirmel J, Bundschuh M, Entling MH, Kowarik I, Buchholz S. Impacts of invasive plants on resident animals across ecosystems, taxa, and feeding types:a global assessment[J]. Global Change Biol, 2016, 22(2):594-603.
[3]	Ricciardi A, Blackburn TM, Carlton JT, Dick JTA, Hulme PE, et al. Invasion science:a horizon scan of emerging challenges and opportunities[J]. Trends Ecol Evol, 2017, 32(6):464-474.
[4]	Si C, Liu X, Wang C, Wang L, Dai Z, et al. Different degrees of plant invasion significantly affect the richness of the soil fungal community[J]. PLoS One, 2013, 8(12):e85490.
[5]	Mamet SD, Lamb EG, Piper CL, Winsley T, Siciliano SD. Archaea and bacteria mediate the effects of native species root loss on fungi during plant invasion[J]. ISME J, 2017, 11(5):1261-1275.
[6]	Cantarel AA, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M, et al. Using plant traits to explain plant-microbe relationships involved in nitrogen acquisition[J]. Ecology, 2015, 96(3):788-799.
[7]	Eisenhauer N, Scheu S, Jousset A. Bacterial diversity stabilizes community productivity[J]. PLoS One, 2012, 7(3):e34517.
[8]	Zhang HY, Goncalves P, Copeland E, Qi SS, Dai ZC, et al. Invasion by the weed Conyza canadensis alters soil nutrient supply and shifts microbiota structure[J]. Soil Biol Biochem, 2020, 143:107739.
[9]	Luo W, Xie Y, Chen X, Li F, Qin X. Competition and facilitation in three marsh plants in response to a water-level gradient[J]. Wetlands, 2010, 30(3):525-530.
[10]	Huang J, Liu M, Chen X, Chen J, Chen F, et al. Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth[J]. Plant Soil, 2013, 367(1):437-447.
[11]	Bardgett RD, Wardle DA. Herbivore-mediated linkages between aboveground and belowground communities[J]. Ecology, 2003, 84(9):2258-2268.
[12]	Schädler M, Alphei J, Scheu S, Brandl R, Auge H. Resource dynamics in an early-successional plant community are influenced by insect exclusion[J]. Soil Biol Biochem, 2004, 36(11):1817-1826.
[13]	Orrock JL, Dutra HP, Marquis RJ, Barber N. Apparent competition and native consumers exacerbate the strong competitive effect of an exotic plant species[J]. Ecology, 2015, 96(4):1052-1061.
[14]	Kong HG, Kim BK, Song GC, Lee S, Ryu CM. Aboveground whitefly infestation-mediated reshaping of the root microbiota[J]. Front Microbiol, 2016, 7:1314.
[15]	Dematheis F, Zimmerling U, Flocco C, Kurtz B, Vidal S, et al. Multitrophic interaction in the rhizosphere of maize:root feeding of western corn rootworm larvae alters the microbial community composition[J]. PLoS One, 2012, 7(5):e37288.
[16]	Wang Y, Ismail M, Huang W, Wang Y, Ding J. Population dynamics and overwintering of a biological control beetle, Agasicles hygrophila, on a nontarget plant Alternanthera sessilis, along a latitudinal gradient[J]. J Pest Sci, 2018, 92(2):835-845.
[17]	Lu X, Siemann E, Shao X, Wei H, Ding J. Climate warming affects biological invasions by shifting interactions of plants and herbivores[J]. Global Change Biol, 2013, 19(8):2339-2347.
[18]	Coulson SJ, Bale JS. Supercooling and survival of the beech leaf mining weevil Rhynchaenus fagi L.(Coleop-tera:Curculionidae)[J]. J Insect Physiol, 1996, 42(7):617-623.
[19]	Lu X, Siemann E, He M, Wei H, Shao X, et al. Climate warming increases biological control agent impact on a non-target species[J]. Ecol Lett, 2015, 18(1):48-56.
[20]	Ma R, Wang R, Ding J. Classical biological control of exotic weeds[J]. Acta Pharmacol Sin, 2003, 23(12):2677-2688.
[21]	Bezemer TM, Harvey JA, Cronin JT. Response of native insect communities to invasive plants[J]. Annual Rev Entomol, 2014, 59:119-141.
[22]	Chen Y, Zhou Y, Yin TF, Liu CX, Luo FL. The invasive wetland plant Alternanthera philoxeroides shows a higher tolerance to waterlogging than its native congener Alternanthera sessilis[J]. PLoS One, 2013, 8(11):e81456.
[23]	Dai H, Lu X, Zhang J, Ding J. Responses of a native beetle to novel exotic plant species with varying invasion history[J]. Ecol Entomol, 2014, 39(1):118-124.
[24]	He M, Zhang J, Siemann E, Yi J, Qin W, et al. Herbivory of a biocontrol agent on a native plant causes an indirect trait-mediated non-target effect on a native insect[J]. J Ecol, 2021, 109(7):2692-2704.
[25]	Qin Z, Xie JF, Quan GM, Zhang JE, Mao DJ, et al. Impacts of the invasive annual herb Ambrosia artemisiifolia L. on soil microbial carbon source utilization and enzymatic activities[J]. Eur J Soil Biol, 2014, 60:58-66.
[26]	Magoc T, Salzberg SL. FLASH:fast length adjustment of short reads to improve genome assemblies[J]. Bioinformatics, 2011, 27(21):2957-2963.
[27]	Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2[J]. Nat Biotechnol, 2019, 37(8):852-857.
[28]	Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome[J]. Science, 2016, 353(6305):1272-1277.
[29]	Team RC. R:A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria[CP/OL]. 2018. https://www.R-project.org.
[30]	Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RG, et al. Vegan:community ecology package. R pac-kage version 2.2-1[CP/OL]. 2013. https://CRAN.R-project.org/package=vegan.
[31]	Hothorn T, Bretz F, Westfall P. Package multcomp:simultaneous inference in general parametric models[CP/OL]. 2015. http://multcomp.R-forge.R-project.org.
[32]	Wickham H, Chang W, Wickham MH. Package ‘ggplot2’. Create elegant data visualisations using the grammar of graphics. Version 3.3-3[CP/OL]. 2016. https://ggplot2.tidyverse.org.
[33]	Stefanowicz AM, Stanek M, Majewska ML, Nobis M, Zubek S. Invasive plant species identity affects soil microbial communities in a mesocosm experiment[J]. Appl Soil Ecol, 2019, 136:168-177.
[34]	Batten KM, Scow KM, Davies KF, Harrison SP. Two invasive plants alter soil microbial community composition in serpentine grasslands[J]. Biol Invasions, 2006, 8(2):217-230.
[35]	Zheng J, Li J, Lan Y, Liu S, Zhou L, et al. Effects of Spartina alterniflora invasion on Kandelia candel rhizospheric bacterial community as determined by high-throughput sequencing analysis[J]. J Soil Sediment, 2018, 19(1):332-344.
[36]	Cao M, Cui L, Sun H, Zhang X, Zheng X, et al. Effects of Spartina alterniflora invasion on soil microbial community structure and ecological functions[J]. Microorganisms, 2021, 9(1):138.
[37]	王文晓. 宁夏草原针茅属植物根际土壤微生物多样性对生态因子响应研究[D]. 银川:宁夏大学, 2020.
[38]	Pineda A, Zheng SJ, van Loon JJ, Pieterse CM, Dicke M. Helping plants to deal with insects:The role of beneficial soil-borne microbes[J]. Trends Plant Sci, 2010, 15(9):507-514.
[39]	Zhou J, Ju R, Li B, Wu J. Responses of soil biota and nitrogen availability to an invasive plant under aboveground herbivory[J]. Plant Soil, 2017, 415(1):479-491.
[40]	Wolfe BE, Klironomos JN. Breaking new ground:soil communities and exotic plant invasion[J]. Bioscience, 2005, 55(6):477-487.
[41]	Rodrigues RR, Pineda RP, Barney JN, Nilsen ET, Barrett JE, et al. Plant invasions associated with change in root-zone microbial community structure and diversity[J]. PLoS One, 2015, 10(10):e0141424.
[42]	Yang JW, Yi HS, Kim H, Lee B, Lee S, et al. Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora[J]. J Ecol, 2011, 99(1):46-56.
[43]	Kong Y, Kong J, Wang D, Huang H, Geng K, et al. Effect of Ageratina adenophora invasion on the composition and diversity of soil microbiome[J]. J Gen Appl Microbiol, 2017, 63(2):114-121.
[44]	Jiang X, Cao L, Zhang R, Yan L, Mao Y, et al. Effects of nitrogen addition and litter properties on litter decomposition and enzyme activities of individual fungi[J]. Appl Soil Ecol, 2014, 80:108-115.
[45]	Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, et al. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling[J]. Microbiome, 2013, 1(1):1-17.
[46]	Song S, Zhang C, Gao Y, Zhu X, Wang R, et al. Responses of wetland soil bacterial community and edaphic factors to two-year experimental warming and Spartina alterniflora invasion in Chongming Island[J]. J Clean Prod, 2020, 250:119502.
[47]	Waite D, Chuvochina M, Pelikan C, Parks DH, Yilmaz P, et al. Proposal to reclassify the Proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities[J]. Int J Syst Evol Micr, 2020, 70(11):5972-6016.
[48]	Lu X, He M, Ding J, Siemann E. Latitudinal variation in soil biota:testing the biotic interaction hypothesis with an invasive plant and a native congener[J]. ISME J, 2018, 12(12):2811-2822.
[49]	Sun S, Li S, Avera BN, Strahm BD, Badgley BD. Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration[J]. Appl Environ Microb, 2017, 83(14):e00966-17.
[50]	Santonja M, Rancon A, Fromin N, Baldy V, Hättenschwiler S, et al. Plant litter diversity increases microbial abundance, fungal diversity, and carbon and nitrogen cycling in a mediterranean shrubland[J]. Soil Biol Biochem, 2017, 111:124-134.
[51]	Drenovsky RE, Batten KM. Invasion by Aegilops triuncialis (Barb Goatgrass) slows carbon and nutrient cycling in a serpentine grassland[J]. Biol Invasions, 2007, 9(2):107-116.

[1]	Wang Jun-Wei, Chen Yong-Hao, La Qiong. Diversity, distribution patterns, and floristic characteristics of seed plants endemic to Tibet, China[J]. Plant Science Journal, 2023, 41(5): 594-603. DOI: 10.11913/PSJ.2095-0837.22298
[2]	Fan Ying-Jie, Liao Yu-Jia, Wang Meng-Zheng, Liu Ling, Song Xiao-Tong, Shao Xiao-Ming. New distribution and distribution prediction of the endemic species Encalypta asiatica J. C. Zhao & L. Li in Tibet, China[J]. Plant Science Journal, 2021, 39(4): 358-366. DOI: 10.11913/PSJ.2095-0837.2021.40358
[3]	Cao Qian, Gao Qing-Bo, Guo Wan-Jun, Zhang Yu, Wang Zhi-Hua, Ma Xiao-Lei, Zhang Fa-Qi, Chen Shi-Long. Impacts of human activities and environmental factors on potential distribution of Swertia przewalskii Pissjauk., an endemic plant in Qing-Tibetan Plateau, using MaxEnt[J]. Plant Science Journal, 2021, 39(1): 22-31. DOI: 10.11913/PSJ.2095-0837.2021.10022
[4]	Li Dan-Qi, Hu Wan, Han Cai-Xia, Chen Lu-Dan, Zhang Zhi-Yong, Zhong Ai-Wen, Wei Zong-Xian, Peng Yan-Song. Prediction of potential suitable distribution of Fokienia hodginsii (Dunn) Henry et Thomas based on MaxEnt model[J]. Plant Science Journal, 2020, 38(6): 743-750. DOI: 10.11913/PSJ.2095-0837.2020.60743
[5]	Zhou Ya-Dong, Mwangi Brian Njoroge, Ndungu John Mbari, Wang Sheng-Wei, Hu Guang-Wan, Wang Qing-Feng. Simulating potential distribution of Afrocanthium (Rubiaceae) in Kenya based on MaxEnt and its application in the Flora of Kenya[J]. Plant Science Journal, 2020, 38(5): 636-643. DOI: 10.11913/PSJ.2095-0837.2020.50636
[6]	Shuayib Yusup, Mamtimin Sulayman, Winira Ilghar, Zhang Zhong-Xin. Prediction of potential distribution of Didymodon (Bryophyta, Pottiaceae) in Xinjiang based on the MaxEnt model[J]. Plant Science Journal, 2018, 36(4): 541-553. DOI: 10.11913/PSJ.2095-0837.2018.40541
[7]	Tao Lian, Yang Wen-Yuan, Xie Hong-Jiang, Pan Cui-Ping, Li Yan-Feng, Li Ju, Huan Yun-Min. Quality evaluation of ‘Golden Delicious’ apple from different ecological regions in Tibet and its response to meteorological factors[J]. Plant Science Journal, 2018, 36(1): 86-93. DOI: 10.11913/PSJ.2095-0837.2018.10086
[8]	JIANG Yan-Bin, ZHANG Yang-Jian. Distribution of Plant Functional Groups in the Natural Grasslands of Xizang, China[J]. Plant Science Journal, 2016, 34(2): 220-229. DOI: 10.11913/PSJ.2095-0837.2016.20220
[9]	WANG Wen-Tsai. Two New Species of Urticaceae from Tibet[J]. Plant Science Journal, 2014, 32(1): 24-26. DOI: 10.3724/SP.J.1142.2014.10024
[10]	YU Jing, TANG Yan-Xue, GUO Shui-Liang. Comparison of the Geographical Distribution of Racomitrium and Grimmia in China Using ArcGis and MaxEnt Software[J]. Plant Science Journal, 2012, 30(5): 443-458. DOI: 10.3724/SP.J.1142.2012.50443

Cited By

Get Citation

PDF

XML

Article views (382) PDF downloads (236)

Turn off MathJax

Article Contents

Abstract

References

Plant competition and insect herbivory mediate the impact of invasive plants on soil bacterial community and function

Abstract

References

Related Articles

Catalog

Plant competition and insect herbivory mediate the impact of invasive plants on soil bacterial community and function

Abstract

References

Related Articles

Catalog

Export File

Citation

Format

Content