CHALLENGES PROVIDING MULTIPLE ECOSYSTEM BENEFITS FOR SUSTAINABLE MANAGED SYSTEMS

Highlights

● For 8000 years, agricultural practices have affected atmospheric CO₂ concentrations.

● Paddy rice cultivation has impacted atmospheric CH₄ concentration since 5000 years ago.

● Modern agricultural practices must include carbon storage and reduced emissions.

● Sustainable management in agriculture must be combined with decarbonizing the economy and reducing population growth.

Abstract

Since humans started practicing agriculture at the expense of natural forests, 8000 years ago, they have affected atmospheric CO₂ concentrations. Their impact on atmospheric CH₄ started about 5000 years ago, as result of the cultivation of paddy rice. A challenge of modern agricultural practices is to reverse the impact cropping has had on greenhouse gas emissions and the global climate. There is an increasing demand for agriculture to provide food security as well as a range of other ecosystem services. Depending on ecosystem management, different practices may involve trade-offs and synergies, and these must be considered to work toward desirable management systems. Solution toward food security should not only focus on agricultural management practices, but also on strategies to reduce food waste, more socially-just distribution of resources, changes in lifestyle including decarbonization of the economy, as well as reducing human population growth.

Graphical abstract

Keywords

crop diversification / ecosystem services / food security / sustainable cropping systems

References

[1] Rockström J, Steffen W, Noone K, Persson A, Chapin F S 3rd, Lambin E F, Lenton T M, Scheffer M, Folke C, Schellnhuber H J, Nykvist B, de Wit C A, Hughes T, van der Leeuw S, Rodhe H, Sörlin S, Snyder P K, Costanza R, Svedin U, Falkenmark M, Karlberg L, Corell R W, Fabry V J, Hansen J, Walker B, Liverman D, Richardson K, Crutzen P, Foley J A. A safe operating space for humanity. Nature, 2009, 461( 7263): 472–475

[2] Hines C. Immigration and population: the interlinked ecological crisis that dares not speak its name. The Ecological Citizen, 2018, 2: 51–55

[3] Cafaro P. Climate ethics and population policy: a review of recent philosophical work. Wiley Interdisciplinary Reviews: Climate Change, 2022, 13 : e748

[4] Queiroz C, Norström A V, Downing A, Harmáčková Z V, De Coning C, Adams V, Bakarr M, Baedeker T, Chitate A, Gaffney O, Gordon L, Hainzelin É, Howlett D, Krampe F, Loboguerrero A M, Nel D, Okollet C, Rebermark M, Rockström J, Smith M, Wabbes-Candotti S, Matthews N. Investment in resilient food systems in the most vulnerable and fragile regions is critical. Nature Food, 2021, 2 : 546–551

[5] Storkey J, Macdonald A J. The role of Long-Term Experiments in validating trait-based approaches to achieving multi-functionality in grasslands. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021438

[6] Lawes J B, Gilbert J H. The Rothamsted Experiments: Being an Account of Some of the Results of the Agricultural Investigations, Conducted at Rothamsted in the Field, the Feeding Shed, and the Laboratory Over a Period of Fifty Years. Highland and Agricultural Society of Scotland, 1895

[7] Lambers H, Poorter H. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research, 1992, 23 : 187–261

[8] Grime J P. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist, 1977, 111( 982): 1169–1194

[9] Tilman D, Reich P B, Knops J, Wedin D, Mielke T, Lehman C. Diversity and productivity in a long-term grassland experiment. Science, 2001, 294( 5543): 843–845

[10] Yu R P, Lambers H, Callaway R M, Wright A J, Li L. Belowground facilitation and trait matching: two or three to tango. Trends in Plant Science, 2021, 26 : 1227–1235

[11] Faucon M P, Houben D, Lambers H. Plant functional traits: soil and ecosystem services. Trends in Plant Science, 2017, 22( 5): 385–394

[12] Ampt E A, van Ruijven J, Zwart M P, Raaijmakers J M, Termorshuizen A J, Mommer L. Plant neighbours can make or break the disease transmission chain of a fungal root pathogen. New Phytologist, 2022, 233( 3): 1303–1316

[13] George T S, Hawes C, Valentine T, Karley A J, Lannetta P P M, Brooker R W. Harnessing ecological principles and physiological mechanisms in diversifying agricultural systems for sustainability: experience from studies deploying nature based solutions in Scotland. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021437

[14] Stockmann U, Adams M A, Crawford J W, Field D J, Henakaarchchi N, Jenkins M, Minasny B, McBratney A B, Courcelles V R, Singh K, Wheeler I, Abbott L, Angers D A, Baldock J, Bird M, Brookes P C, Chenu C, Jastrow J D, Lal R, Lehmann J, O’Donnell A G, Parton W J, Whitehead D, Zimmermann M. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agriculture, Ecosystems & Environment, 2013, 164 : 80–99

[15] Cong W F, Suriyagoda L D B, Lambers H. Tightening the phosphorus cycle through phosphorus-efficient crop genotypes. Trends in Plant Science, 2020, 25( 10): 967–975

[16] Gatiboni L, Brunetto G, Pavinato P S, George T S. Legacy phosphorus in agriculture: role of past management and perspectives for the future. Frontiers of Earth Science, 2020, 8 : 619935

[17] Resh S C, Binkley D, Parrotta J A. Greater soil carbon sequestration under nitrogen-fixing trees compared with Eucalyptus species. Ecosystems, 2002, 5 : 217–231

[18] Nge F J, Cambridge M L, Ellsworth D S, Zhong H, Lambers H. Cluster roots are common in Daviesia and allies (Mirbelioids; Fabaceae). Journal of the Royal Society of Western Australia, 2020, 103 : 111–118

[19] Gardner W K, Barber D A, Parbery D G. The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil, 1983, 70 : 107–124

[20] Arahou M, Diem H G. Iron deficiency induces cluster (proteoid) root formation in Casuarina glauca. Plant and Soil, 1997, 196: 71−79

[21] Reddell P, Yun Y, Shipton W A. Cluster roots and mycorrhizae in Casuarina cunninghamiana: their occurrence and formation in relation to phosphorus supply. Australian Journal of Botany, 1997, 45( 1): 41–51

[22] Anderson D M W, Morrison N A. Identification of Albizia gum exudates which are not permitted food additives. Food Additives and Contaminants, 1990, 7( 2): 175–180

[23] Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan M H, Ranathunge K, Siddique K H M. The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytologist, 2018, 219( 2): 518–529

[24] Lambers H, Hayes P E, Laliberté E, Oliveira R S, Turner B L. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends in Plant Science, 2015, 20( 2): 83–90

[25] Ding W, Cong W F, Lambers H. Plant phosphorus-acquisition and -use strategies affect soil carbon cycling. Trends in Ecology & Evolution, 2021, 36( 10): 899–906

[26] Son Y, Stott K, Manning D A C, Cooper J M. Carbon sequestration in artificial silicate soils facilitated by arbuscular mycorrhizal fungi and glomalin-related soil protein. European Journal of Soil Science, 2021, 72( 2): 863–870

[27] Rillig M C. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters, 2004, 7( 8): 740–754

[28] Zhong H, Zhou J. Response to Ding et al.: carboxylate exudation promotes C sequestration in dryland ecosystems. Trends in Ecology & Evolution, 2022, 37( 1): 12–13

[29] Berner R A. Weathering, plants, and the long-term carbon cycle. Geochimica et Cosmochimica Acta, 1992, 56( 8): 3225–3231

[30] Liu Z. Is pedogenic carbonate an important atmospheric CO₂ sink. Chinese Science Bulletin, 2011, 56( 35): 3794–3796

[31] Ding W, Cong W F, Lambers H. Response to Zhong and Zhou: P-acquisition strategies and total soil C sequestration. Trends in Ecology & Evolution, 2022, 37( 1): 14–15

[32] Raven J A. Interactions between above and below ground plant structures: mechanisms and ecosystem services. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021.33

[33] Lal R, Smith P, Jungkunst H F, Mitsch W J, Lehmann J, Nair P K R, McBratney A B, de Moraes Sá J C, Schneider J, Zinn Y L, Skorupa A L A, Zhang H L, Minasny B, Srinivasrao C, Ravindranath N H. The carbon sequestration potential of terrestrial ecosystems. Journal of Soil and Water Conservation, 2018, 73( 6): 145A–152A

[34] Tvinnereim E, Mehling M. Carbon pricing and deep decarbonisation. Energy Policy, 2018, 121 : 185–189

[35] Höhne N, Gidden M J, den Elzen M, Hans F, Fyson C, Geiges A, Jeffery M L, Gonzales-Zuñiga S, Mooldijk S, Hare W, Rogelj J. Wave of net zero emission targets opens window to meeting the Paris Agreement. Nature Climate Change, 2021, 11 : 820–822

[36] Zhang S, Yun W, Xia Y, Wu S, You Z, Rillig M C. Arbuscular mycorrhiza reduced nitrogen loss via runoff, leaching, and emission of N₂O and NH₃ from microcosms of paddy fields. Water, Air, and Soil Pollution, 2022, 233 : 11

[37] Oehler F, Bordenave P, Durand P. Variations of denitrification in a farming catchment area. Agriculture, Ecosystems & Environment, 2007, 120( 2-4): 313–324

[38] Lodhi M A K, Killingbeck K T. Allelopathic inhibition of nitrification and nitrifying bacteria in a ponderosa pine (Pinus ponderosa Dougl.) community. American Journal of Botany, 1980, 67( 10): 1423–1429

[39] Gasser J K R. Nitrification inhibitors their occurrence, production and effects of their use on crop yields and composition. Soils and Fertilizers, 1970, 33 : 547–554

[40] Lodhi M A K. Comparative inhibition of nitrifiers and nitrification in a forest community as a result of the allelopathic nature of various tree species. American Journal of Botany, 1978, 65( 10): 1135–1137

[41] White C S. Volatile and water-soluble inhibitors of nitrogen mineralization and nitrification in a ponderosa pine ecosystem. Biology and Fertility of Soils, 1986, 2 : 97–104

[42] Subbarao G V, Ishikawa T, Ito O, Nakahara K, Wang H Y, Berry W L. A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant and Soil, 2006, 288: 101−112

[43] Gopalakrishnan S, Subbarao G V, Nakahara K, Yoshihashi T, Ito O, Maeda I, Ono H, Yoshida M. Nitrification Inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. Journal of Agricultural and Food Chemistry, 2007, 55( 4): 1385–1388

[44] Subbarao G V, Rondon M, Ito O, Ishikawa T, Rao I M, Nakahara K, Lascano C, Berry W L. Biological nitrification inhibition (BNI)—is it a widespread phenomenon?. Plant and Soil, 2007, 294 : 5–18

[45] O’Sullivan C A, Duncan E G, Roper M M, Richardson A E, Kirkegaard J A, Peoples M B. Root exudates from canola exhibit biological nitrification inhibition and are effective in inhibiting ammonia oxidation in soil. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021421

[46] Hedden P. The genes of the Green Revolution. Trends in Genetics, 2003, 19( 1): 5–9

[47] Pellegrini P, Fernández R J. Crop intensification, land use, and on-farm energy-use efficiency during the worldwide spread of the green revolution. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115( 10): 2335–2340

[48] Hunke P, Mueller E N, Schröder B, Zeilhofer P. The Brazilian Cerrado: assessment of water and soil degradation in catchments under intensive agricultural use. Ecohydrology, 2015, 8( 6): 1154–1180

[49] Peñuelas J, Janssens I A, Ciais P, Obersteiner M, Sardans J. Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health. Global Change Biology, 2020, 26( 4): 1962–1985

[50] Groot J C J, Yang X. Trade-offs in the design of sustainable cropping systems at the regional level—an analysis in the North China Plain. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021434

[51] Cooledge E C, Chadwock D R, Leake J R, Jones D L. Agronomic and environmental benefits of reintroducing herb- and legume-rich multispecies leys into arable rotations: a review. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi:10.15302/J-FASE-2021439

[52] Singh D, Mathimaran N, Boller T, Kahmen A. Deep-rooted pigeon pea promotes the water relations and survival of shallow-rooted finger millet during drought-Despite strong competitive interactions at ambient water availability. PLoS One, 2020, 15( 2): e0228993

[53] Pang J, Wang Y, Lambers H, Tibbett M, Siddique K H M, Ryan M H. Commensalism in an agroecosystem: hydraulic redistribution by deep-rooted legumes improves survival of a droughted shallow-rooted legume companion. Physiologia Plantarum, 2013, 149( 1): 79–90

[54] Thorup-Kristensen K, Halberg N, Nicolaisen M, Olesen J E, Crews T E, Hinsinger P, Kirkegaard J, Pierret A, Dresbøll D B. Digging deeper for agricultural resources, the value of deep rooting. Trends in Plant Science, 2020, 25( 4): 406–417

[55] McNally S R, Laughlin D C, Rutledge S, Dodd M B, Six J, Schipper L A. Root carbon inputs under moderately diverse sward and conventional ryegrass-clover pasture: implications for soil carbon sequestration. Plant and Soil, 2015, 392 : 289–299

[56] Nuruzzaman M, Lambers H, Bolland M D A, Veneklaas E J. Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant and Soil, 2005, 271: 175–187

[57] Jemo M, Abaidoo R C, Nolte C, Tchienkoua M, Sanginga N, Horst W J. Phosphorus benefits from grain-legume crops to subsequent maize grown on acid soils of southern Cameroon. Plant and Soil, 2006, 284 : 385–397

[58] de Tombeur F, Cornelis J T, Lambers H. Silicon mobilisation by root-released carboxylates. Trends in Plant Science, 2021, 26( 11): 1116–1125

[59] de Tombeur F, Roux P, Cornelis J T. Silicon dynamics through the lens of soil-plant-animal interactions: perspectives for agricultural practices. Plant and Soil, 2021, 467 : 1–28

[60] Laurance W F, Sayer J, Cassman K G. Agricultural expansion and its impacts on tropical nature. Trends in Ecology & Evolution, 2014, 29( 2): 107–116

[61] Kervroëdan L, Houben D, Guidet J, Denier J, Dulaurent A M, Marraccini E, Deligey A, Journel C, Lamerrec J, Faucon M P. Agri-environmental assessment of conventional and alternative bioenergy cropping systems promoting biomass productivity. Frontiers of Agricultural Science and Engineering, 2022 [Published Online] doi: 10.15302/J-FASE-2021435

[62] Lynch J P, Wojciechowski T. Opportunities and challenges in the subsoil: pathways to deeper rooted crops. Journal of Experimental Botany, 2015, 66( 8): 2199–2210

[63] Jasinskas A, Zaltauskas A, Kryzeviciene A. The investigation of growing and using of tall perennial grasses as energy crops. Biomass and Bioenergy, 2008, 32( 11): 981–987

[64] Dubis B, Jankowski K J, Sokólski M M, Załuski D, Bórawski P, Szempliński W. Biomass yield and energy balance of fodder galega in different production technologies: an 11-year field experiment in a large-area farm in Poland. Renewable Energy, 2020, 154 : 813–825

[65] Otto I M, Donges J F, Cremades R, Bhowmik A, Hewitt R J, Lucht W, Rockström J, Allerberger F, McCaffrey M, Doe S S P, Lenferna A, Morán N, van Vuuren D P, Schellnhuber H J. Social tipping dynamics for stabilizing Earth’s climate by 2050. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117( 5): 2354–2365

[66] Eaton E. Approaches to energy transitions: carbon pricing, managed decline, and/or green new deal. Geography Compass, 2021, 15( 2): e12554

[67] Scovronick N, Budolfson M B, Dennig F, Fleurbaey M, Siebert A, Socolow R H, Spears D, Wagner F. Impact of population growth and population ethics on climate change mitigation policy. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114( 46): 12338–12343

[68] Fleurbaey M, Ferranna M, Budolfson M, Dennig F, Mintz-Woo K, Socolow R, Spears D, Zuber S. The social cost of carbon: valuing inequality, risk, and population for climate policy. The Monist, 2019, 102 : 84–109

[69] Benton T G, Bailey R. The paradox of productivity: agricultural productivity promotes food system inefficiency. Global Sustainability, 2019, 2 : e6

Acknowledgements

This work was funded by the National Natural Science Foundation of China (32072676), and the Program of Advanced Discipline Construction in Beijing (Agriculture Green Development).

Compliance with ethics guidelines

Hans Lambers and Wen-Feng Cong declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any study with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2022. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)