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Predation on weed seeds and seedlings by Pheretima guillelmi and its potential for weed biocontrol

Published online by Cambridge University Press:  26 August 2020

Tao Li Open the ORCID record for Tao Li [Opens in a new window] ,
Jiequn Fan ,
Zhenguan Qian ,
Guohui Yuan ,
Dandan Meng ,
Shuiliang Guo Open the ORCID record for Shuiliang Guo [Opens in a new window]  and
Weiguang Lv Open the ORCID record for Weiguang Lv [Opens in a new window]
Tao Li
Affiliation:
Associate Professor, Shanghai Academy of Agricultural Sciences, Shanghai, China
Jiequn Fan
Affiliation:
Associate Professor, Shanghai Academy of Agricultural Sciences, Shanghai, China
Zhenguan Qian
Affiliation:
Associate Professor, Shanghai Academy of Agricultural Sciences, Shanghai, China
Guohui Yuan
Affiliation:
Assistant Professor, Shanghai Academy of Agricultural Sciences, Shanghai, China
Dandan Meng
Affiliation:
Graduate Student, Shanghai Normal University, Shanghai, China
Shuiliang Guo*
Affiliation:
Professor, Shanghai Normal University, Shanghai, China
Weiguang Lv*
Affiliation:
Professor, Shanghai Academy of Agricultural Sciences, Shanghai, China
*
Authors for correspondence: Shuiliang Guo, Shanghai Normal University, Guilin Road, no. 100, Shanghai, 200234, China. (Email: [email protected]); and Weiguang Lv, Shanghai Academy of Agricultural Sciences, 1000 Jinqi Road, Fengxian District, Shanghai, 201403, China. (Email: [email protected]).
Authors for correspondence: Shuiliang Guo, Shanghai Normal University, Guilin Road, no. 100, Shanghai, 200234, China. (Email: [email protected]); and Weiguang Lv, Shanghai Academy of Agricultural Sciences, 1000 Jinqi Road, Fengxian District, Shanghai, 201403, China. (Email: [email protected]).
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Abstract

The soil weed seedbank is the source of future weed infestations. Seed predation can result in a large number of seed losses, thus contributing to weed biocontrol. Earthworms are important predators of seeds and seedlings and affect seeds and seedling survival after gut passage. A study was conducted to assess the ability of Pheretima guillelmi (Kinberg) to ingest and digest the seeds and seedlings of 15 main farmland weed species. Pheretima guillelmi ingested the seeds and seedlings of each weed species tested. The percentages of seeds and seedlings ingested were 96.7% to 100% and 21.7% to 94.2%, respectively. Pheretima guillelmi showed greater ingestion of seeds than seedlings for each species and digested the seeds and seedlings of each weed species tested to varying extents. The percentages of seeds and seedlings digested were less than 15% irrespective of the weed species. Passage through the gut of P. guillelmi affected the survival of seeds and seedlings. The germination of large crabgrass [Digitaria sanguinalis (L.) Scop.], green foxtail [Setaria viridis (L.) P. Beauv.], goosegrass [Eleusine indica (L.) Gaertn.], Chinese sprangletop [Leptochloa chinensis (L.) Nees], Malabar sprangletop [Leptochloa fusca (L.) Kunth], redroot pigweed (Amaranthus retroflexus L.), common purslane (Portulaca oleracea L.), barnyardgrass [Echinochloa crus-galli (L.) P. Beauv.], and ricefield flatsedge (Cyperus iria L.) seeds egested by P. guillelmi decreased by 46%, 49%, 47%, 25%, 38%, 26%, 32%, 13%, and 15%, respectively, compared with their respective controls. In contrast to seed ingestion, ingestion of seedlings by P. guillelmi was fatal to individuals of all weed species; no seedlings survived passage through the gut. Our results indicate that predation of weed seeds and seedlings by P. guillelmi probably depletes the soil weed seedbank and that the introduction of P. guillelmi into fields is a potential strategy for weed biocontrol in farmland.

Keywords

Earthwormsseed and seedling predatorssoil seedbankweed management
Type
Research Article
Information
Weed Science , Volume 68 , Issue 6 , November 2020 , pp. 639 - 645
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of the Weed Science Society of America

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Footnotes

*

These authors contributed equally to this work.

Associate Editor: Steven S. Seefeldt, Washington State University

References

Aira, M, Piearce, TG (2009) The earthworm Lumbricus terrestris favours the establishment of Lolium perenne over Agrostis capillaris seedlings through seed consumption and burial. Appl Soil Ecol 41:360–363 CrossRefGoogle Scholar
Arif, M, Ali, K, Haq, MS, Khan, Z (2013) Biochar, fym and nitrogen increases weed infestation in wheat. Pak J Weed Sci Res 19:411–418 Google Scholar
Baraibar, B, Carrión, E, Recasens, J, Westerman, PR (2011) Unravelling the process of weed seed predation: developing options for better weed control. Biol Control 56:85–90 10.1016/j.biocontrol.2010.09.010CrossRefGoogle Scholar
Berg, H (2002) Rice monoculture and integrated rice-fish farming in the Mekong Delta, Vietnam—economic and ecological considerations. Ecol Econ 41:95–107 10.1016/S0921-8009(02)00027-7CrossRefGoogle Scholar
Berg, H, Tam, NT (2018) Decreased use of pesticides for increased yields of rice and fish—options for sustainable food production in the Mekong Delta. Sci Total Environ 619–620:319–327 CrossRefGoogle ScholarPubMed
Chauhan, BS, Johnson, DE (2010) The role of seed ecology in improving weed management strategies in the tropics. Adv Agron 105:221–262 10.1016/S0065-2113(10)05006-6CrossRefGoogle Scholar
Curry, JP, Schmidt, O (2007) The feeding ecology of earthworms—a review. Pedobiologia (Jena) 50:463–477 10.1016/j.pedobi.2006.09.001CrossRefGoogle Scholar
Decaëns, T, Mariani, L, Betancourt, N, Jiménez, JJ (2003) Seed dispersion by surface casting activities of earthworms in Colombian grasslands. Acta Oecologica 24:175–185 10.1016/S1146-609X(03)00083-3CrossRefGoogle Scholar
Dicke, D, Gerhards, R (2006) The impact of post harvest weed seed predation compared to stubble cultivation on weed seed decline. J Plant Dis Prot Special Is(20):267–272 Google Scholar
Dobson, AM, Blossey, B, Richardson, JB (2017) Invasive earthworms change nutrient availability and uptake by forest understory plants. Plant Soil 421:175–190 10.1007/s11104-017-3412-9CrossRefGoogle Scholar
Edwards, CA, Bohlen, PJ (1996) Biology and ecology of earthworms. 3rd ed. London: Chapman & Hall. 426 pGoogle Scholar
Eisenhauer, N, Butenschoen, O, Radsick, S, Scheu, S (2010) Earthworms as seedling predators: importance of seeds and seedlings for earthworm nutrition. Soil Biol Biochem 42:1245–1252 10.1016/j.soilbio.2010.04.012CrossRefGoogle Scholar
Eisenhauer, N, Schuy, M, Butenschoen, O, Scheu, S (2009) Direct and indirect effects of endogeic earthworms on plant seeds. Pedobiologia (Jena) 52:151–162 10.1016/j.pedobi.2008.07.002CrossRefGoogle Scholar
Ekeleme, F, Akobundu, IO, Isichei, AO, Chikoye, D (2003) Cover crops reduce weed seedbanks in maize–cassava systems in southwestern Nigeria. Weed Sci 51:774–780 10.1614/0043-1745(2003)051[0774:CCRWSI]2.0.CO;2CrossRefGoogle Scholar
Elmer, WH (2009) Influence of earthworm activity on soil microbes and soilborne diseases of vegetables. Plant Dis 93:175–179 10.1094/PDIS-93-2-0175CrossRefGoogle ScholarPubMed
Fartyal, D, Agarwal, A, James, D, Borphukan, B, Ram, B, Sheri, V, Agrawal, PK, Achary, VMM, Reddy, MK (2018) Developing dual herbicide tolerant transgenic rice plants for sustainable weed management. Sci Rep 8:11598 CrossRefGoogle ScholarPubMed
Firbank, LG, Watkinson, AR (1985) A model of interference within plant monocultures. J Theor Biol 116:291–311 10.1016/S0022-5193(85)80269-1CrossRefGoogle Scholar
Forey, E, Barot, S, Decaëns, T, Langlois, E, Laossi, KR, Margerie, P, Scheu, S, Eisenhauer, N (2011) Importance of earthworm-seed interactions for the composition and structure of plant communities: a review. Acta Oecologica 37:594–603 10.1016/j.actao.2011.03.001CrossRefGoogle Scholar
Fründ, HC, Butt, K, Capowiez, Y, Eisenhauer, N, Emmerling, C, Ernst, G, Potthoff, M, Schädler, M, Schrader, S (2010) Using earthworms as model organisms in the laboratory: recommendations for experimental implementations. Pedobiologia (Jena) 53:119–125 10.1016/j.pedobi.2009.07.002CrossRefGoogle Scholar
García-Pérez, JA, Alarcón-Gutiérrez, E, Perroni, Y, Barois, I (2014) Earthworm communities and soil properties in shaded coffee plantations with and without application of glyphosate. Appl Soil Ecol 83:230–237 10.1016/j.apsoil.2013.09.006CrossRefGoogle Scholar
Ghersa, CM, Benech-Arnold, RL, Satorre, EH, Martínez-Ghersa, MA (2000) Advances in weed management strategies. Field Crops Res 67:95–104 CrossRefGoogle Scholar
Grant, JD (1983) The activities of earthworms and the fates of seeds. Pages 107–122 in Satchell, JE, ed. Earthworm Ecology. Springer, Dordrecht, Netherlands Google Scholar
Holmes, RJ, Froud-Williams, RJ (2005) Post-dispersal weed seed predation by avian and non-avian predators. Agric Ecosyst Environ 105:23–27 10.1016/j.agee.2004.06.005CrossRefGoogle Scholar
Jones, CG, Lawton, JH, Shachak, M (1994) Organisms as ecosystem engineers. Oikos 69:373 10.2307/3545850CrossRefGoogle Scholar
José-María, L, Sans, FX (2011) Weed seedbanks in arable fields: effects of management practices and surrounding landscape. Weed Res 51:631–640 10.1111/j.1365-3180.2011.00872.xCrossRefGoogle Scholar
Kaur, S, Kaur, R, Chauhan, BS (2018) Understanding crop-weed-fertilizer-water interactions and their implications for weed management in agricultural systems. Crop Prot 103:65–72 10.1016/j.cropro.2017.09.011CrossRefGoogle Scholar
Laossi, KR, Noguera, DC, Barot, S (2010) Earthworm-mediated maternal effects on seed germination and seedling growth in three annual plants. Soil Biol Biochem 42:319–323 10.1016/j.soilbio.2009.11.010CrossRefGoogle Scholar
Li, Y, Wang, S, Lu, M, Zhang, Z, Chen, M, Li, S, Cao, R (2019) Rhizosphere interactions between earthworms and arbuscular mycorrhizal fungi increase nutrient availability and plant growth in the desertification soils. Soil Tillage Res 186:146–151 10.1016/j.still.2018.10.016CrossRefGoogle Scholar
Marhan, S, Scheu, S (2005) Effects of sand and litter availability on organic matter decomposition in soil and in casts of Lumbricus terrestris L. Geoderma 128:155–166 CrossRefGoogle Scholar
McRill, M (1974) The ingestion of weed seed by earthworms. Pages 519–524 in Proceedings of the 12th British Weed Control Conference. British Crop Protection Council, LondonGoogle Scholar
Milcu, A, Schumacher, J, Scheu, S (2006) Earthworms (Lumbricus terrestris) affect plant seedling recruitment and microhabitat heterogeneity. Funct Ecol 20:261–268 CrossRefGoogle Scholar
Mills, CH, Gordon, CE, Letnic, M (2018) Rewilded mammal assemblages reveal the missing ecological functions of granivores. Funct Ecol 32:475–485 CrossRefGoogle Scholar
Navntoft, S, Wratten, SD, Kristensen, K, Esbjerg, P (2009) Weed seed predation in organic and conventional fields. Biol Control 49:11–16 10.1016/j.biocontrol.2008.12.003CrossRefGoogle Scholar
Piearce, TG, Roggero, N, Tipping, R (1994) Earthworms and seeds. J Biol Educ 28:195–202 CrossRefGoogle Scholar
Primot, S, Valantin-Morison, M, Makowski, D (2006) Predicting the risk of weed infestation in winter oilseed rape crops. Weed Res 46:22–33 10.1111/j.1365-3180.2006.00489.xCrossRefGoogle Scholar
Rahman, A, James, TK, Mellsop, JM, Grbavac, N (2003) Relationship between soil seedbank and field populations of grass weeds in maize. Pages 215–219 in New Zealand Plant Protection. New Zealand Plant Protection Society, Auckland, NZCrossRefGoogle Scholar
Reiserer, RS, Schuett, GW, Greene, HW (2018) Seed ingestion and germination in rattlesnakes: overlooked agents of rescue and secondary dispersal. Proc R Soc Lond B Biol Sci 285:20172755 Google ScholarPubMed
Sarabi, V (2019) Factors that influence the level of weed seed predation: a review. Weed Biol Manag 19:61–74 CrossRefGoogle Scholar
Scheu, S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia (Jena) 47:846–856 Google Scholar
Shumway, DL, Koide, RT (1994) Seed preferences of Lumbricus terrestris L. Appl Soil Ecol 1:11–15 Google Scholar
Smith, RG, Gross, KL, Januchowski, S (2005) Earthworms and weed seed distribution in annual crops. Agric Ecosyst Environ 108:363–367 CrossRefGoogle Scholar
Subler, S, Baranski, CM, Edwards, CA (1997) Earthworm additions increased short-term nitrogen availability and leaching in two grain-crop agroecosystems. Soil Biol Biochem 29:413–421 CrossRefGoogle Scholar
Tauseef, M, Ihsan, F, Nazir, W, Farooq, J (2012) Weed flora and importance value index (IVI) of the weeds in cotton crop fields in the region of Khanewal, Pakistan. J Weed Sci Res 18:319–330 Google Scholar
Thompson, K, Grime, JP (1979) Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. J Ecol 67:893 CrossRefGoogle Scholar
Vissoh, P V., Gbèhounou, G, Ahanchédé, A, Kuyper, TW, Röling, NG (2004) Weeds as agricultural constraint to farmers in Benin: results of a diagnostic study. NJAS—Wageningen J Life Sci 52:305–329 CrossRefGoogle Scholar
Wang, YS (1999) Environmental impact of herbicide use in the subtropics. Food Sci Agric Chem 1:165–179 Google Scholar
Westerman, PR, Borza, JK, Andjelkovic, J, Liebman, M, Danielson, B (2008) Density-dependent predation of weed seeds in maize fields. J Appl Ecol 45:1612–1620 CrossRefGoogle Scholar
Wyse, DL (1994) New technologies and approaches for weed management in sustainable agriculture systems. Weed Technol 8:403–407 CrossRefGoogle Scholar
Zaller, JG, Saxler, N (2007) Selective vertical seed transport by earthworms: implications for the diversity of grassland ecosystems. Eur J Soil Biol 43(S1):S86–S91 10.1016/j.ejsobi.2007.08.010CrossRefGoogle Scholar
Zheng, X, Lv, W, Song, K, Li, S, Zhang, H, Bai, N, Zhang, J (2018) Effects of a vegetable-eel-earthworm integrated planting and breeding system on bacterial community structure in vegetable fields. Sci Rep 8:9520 CrossRefGoogle ScholarPubMed
Zheng, XQ, Fan, XF, Zhang, HL, Shuang-Xi, LI, Wang, JQ, Zhang, JQ, Wang, LJ, Bin, Tao X, Wei-Guang, L (2015) Effects of Pheretima guillelmi cultivation time on microbial community diversity and characteristics of carbon metabolism in vegetable soil. J Agric Resour Environ 32:596–602 Google Scholar
Zhu, J, Wang, J, DiTommaso, A, Zhang, C, Zheng, G, Liang, W, Islam, F, Yang, C, Chen, X, Zhou, W (2020) Weed research status, challenges, and opportunities in China. Crop Prot 134:104449 CrossRefGoogle Scholar