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Project titleRole of invertebrates in the reduction of greenhouse gas emissions and increase of climatic and environmental safety of rice production in Russia

Research area 04 - BIOLOGY AND LIFE SCIENCES, 04-107 - Ecology of biological systems

KeywordsRice, rice paddies, greenhouse gases, methane, detrital foodwebs, soil invertebrates, environmental and climatic safety, carbon turnover, sustainable agriculture

Annotation
Active recovery of rice production and its intensification in Russia during the past few years increase climatic and toxic loads on the areas of rice production. More than 10% growth of the area occupied by rice in combination with the strong increase of yields in 2006-2014 resulted in the total harvest exceeding 1 million tons in the country. This is achieved by constantly increasing input of fertilizers, pesticides and herbicides what results in the almost complete vanishing of metazoan organisms from the rice paddies and their environs. At the same time one observes exponential growth of GHG emissions from the inundated rice paddies during rice-production season. It is mainly carbon dioxide, methane and to a smaller extent nitrogen oxides which are emitted. The latter two gases have tremendously high Global warming potential (12 and 114 for CH4 and N2O relative to CO2 respectively). Such trends created unacceptable risks for both climate and functional stability of landscapes in rice production areas. That’s why along with the task of increasing food security of the country, it is important to resolve the problem of securing environmental and climatic safety of rice production in Russia. Research of the approaches to increase environmental and climatic safety of rice production becomes even more actual in light of the ongoing agricultural intentsification and increase of seeded area, which are particularly evident in the rice production (see Decision of the Government of Russian Federation No 717 on 14.07.2012). In this framework it is potentially beneficial to use existing natural ecosystem mechanisms of methanogenesis suppression and other GHG (N2O and CO2) emissions mitigation. The considerable potential of GHG emission reduction, biogenic elements reintegration from the rice straw and increasing rice production sustainability is associated with the invertebrate fauna inhabiting rice paddies and its environs. Despite its quite modest direct input into the processes of carbon, nitrogen and other biogenic elements, invertebrates play an important role in regulating activity, production and biomass of microbial compartments of detrital foodwebs which are in turn responsible for 95% of GHG emissions from the rice paddies. Besides that soil animals and earthworms at first place, play an important role in preparing rice straw for decomposition by microorganisms as well as reintegration of carbon accumulated in plant green biomass (which is currently mainly burned) back into soil. As a result it is getting possible to increase soil quality and natural fertility by biological methods. The project aims at investigating the scientific problem of biological regulation of GHG emissions and consecutively soil carbon loss mitigation in the conditions of overmoistened habitats on the example of rice paddies. The major task of the project is justification of the overall GHG and black carbon emissions reduction in the rice production territories by the application of biological methods for the sake of increasing environmental and climatic safety of rice growth at the territory of Russia. Several particular tasks will be solved in relation to this: 1. To analyze soil-dwelling invertebrate communities and the emission of major GHGs in the natural habitats and rice paddies in the three major rice production regions (Kuban river lowland, Caspian sea lowland and Primorsky Krai, Russian Far East). 2. To estimate and quantify the input of soil animals into the process of biogenic elements reintegration during rice straw degradation. 3. To discover and estimate the importance of indigenous invertebrate species as ecosystem engineers, abundance manipulation of which on the rice paddies may have the highest potential of carbon stabilization in soil. The particular emphasis should be made on mitigating GHG emissions during the entire cycle of inundating and drainage of rice paddies. 4. To assess the role of soil invertebrates in various climatic and edaphic conditions in sustaining natural soil fertility and hence rice yields increase due to biogenic elements reintegration from rice straw. 5. To assess the role of soil invertebrates in reducing overall Global warming potential in the gice production regions in Russia. Model areas and methods We are planning to conduct our research in the three model regions in Russia which traditionally practicing rice production. These are: Krasnodarsky Krai, Kalmykia Republic and Primorsky Krai. These territories represent the whole range of natural conditions suitable for rice production in Russia. The major methods of the survey will be: 1) conducting literature results metaanalysis and generalization of best expert opinions on the effectiveness of different soil invertebrate taxa as stabilizers of soil carbon and reintegrators of biogenic elements from rice straw; 2) laboratory experiments in mesocosms for assessment of the role of soil invertebrates in mitigating GHG emissions and reintegrating biogenic elements from the rice straw into soil; 3) field experiment in mesocosms in rice paddies of the three model regions to confirm results of laboratory experiments in nature; 4) modeling elements and energy flow with the best available detrital foodweb models and other advancedtechniques of data processing. Logical model of the project. Based on the tasks of the project the following logical model of the project research intervention is proposed. 1. For discovering the most functionally important soil animals, which potentially have the highest ability of carbon and nitrogen sequestration and reintegration into rice paddy soil, we will conduct literature analysison the topic for the broad spectrum of wet overmoistened habitats. Data systematization and generalizing best expert judgements will result in creating of a “long list” of soil invertebrate taxa which are able to survive inundation in the rice paddies and safeguard highest GHG emissions reduction. Along with that we will study soil fauna in the rice paddies and their environs in the model regions for preparing a “short list” of invertebrates (fulfilling Task 1). 2. Functional significance of these animals as stabilizers of carbon and other biogenic elements in rice paddy soils will be checked in two laboratory experiments on studying rice straw degradation and reduction of GHG emission under different soil humidity levels which simulate conditions during rice growing and after its harvest (fulfilling Tasks 2 and 3). 3. The results achieved will be checked for the most promising invertebrate taxon in a one-year-long field experiment (fulfilling Task 4). 4. Knowledge and results which we will receive will be further used for generating recommendations on the use of soil invertebrates for conservation of natural soil fertility and increasing climatic and environmental safety of rice production (fulfilling Task 5).

Expected results
We expect to resolve an important fundamental problem of assessing the role of soil animals in regulating and stabilizing carbon flow and GHG emission. In the result of the 1-st year work (literature and expert opinions metaanalysis, field soil zoological survey) we will make an inventory of fauna and population of soil invertebrates in the rice paddies and their environs within the three model regions. We shall make a justified “long list” of invertebrate taxa that potentially bear the highest effectiveness of carbon and nitrogen deposition and GHG emission reduction from the rice paddy soil. In the result of the 2-nd year investigations (laboratory experiments) we will define soil animals which are most efficient in stabilizing soil carbon and nitrogen in rice paddy soils and inhibiting GHG emission. “Short lists” of such taxa will be compiled for each of model regions. In the result of the 3-rd year (field experiment) we will quantify the role of model soil invertebrate in reducing GHG emissions from the rice paddies and maintaining natural soil fertility. Besides that as result of the entire project we shall conduct complex modeling of the action of selected model organisms on the balance of GHGs in the rice paddies. Synthesis of all preceding results will be published as recommendations for manipulate soil invertebrate abundance in the rice paddies for increasing climatic and environmental safety of rice production. These results do not have equivalents in the world’s science and will be very innovative.

Annotation of the results obtained in 2018
The project in 2018 entered its final phase. The main tasks for the third year of work were the completion of the analysis of the collected field data on the role of soil animals in the processes of destruction of rice straw and reducing greenhouse gas emissions from rice soils. In parallel, the task of developing recommendations on the use of biological systems for the destruction of rice straw and a parallel increase in soil fertility was solved. According to the results of the synthesis of field and laboratory experiments, it has been convincingly shown that earthworms moderately reduce greenhouse gas emissions, but at the same time stabilize soil carbon (https://doi.org/10.1016/j.ejsobi.2018.10.003). Enchytraeids, on the contrary, do not reliably accelerate the decomposition rate of rice straw, but significantly reduce greenhouse gas emissions by 25%. This indicates their significant role in regulating the activity of the bacterial community on rice paddies, which is especially important in the context of periodic flooding of rice paddies and the reduction of the abundance and activity of true soil animals (micro- and mesoarthropods). On the basis of the studies , general recommendations were formulated on the use of soil animals to increase the sustainability of rice growing under conditions of periodic flooding and the crop rotation practiced both in Russia and increasingly overseas, including alternating flooded (rice) and non-flooded (corn, wheat, soybeans and soybeans) cultures. In particular, four basic principles have been proposed: (a) to increase the efficiency of the process of sequestering greenhouse gas emissions from rice paddies, apply multi-species systems including earthworms, enchitreids, and ground-dwelling arthropods: centipedes and isopods. At the same time, the complementarity of these groups is convincingly shown, as well as the relatively important role of enchytraeids in conditions of flooding, and earthworms and arthropods in the drained paddies. (b) The efficiency of earthworms for the decomposition of straw is highest at a humidity level of 25-50% of the maximum water holding capacity at the simultaneous ability to sequester carbon from straw in the soil (https://doi.org/10.1016/j.ejsobi.2018.10.003). (c) Biological systems for the decomposition of straw with the involvement of upland crops are most effective in light (sandy) soils due to better aeration of the substrate. (d) It is more expedient to decompose rice straw in bioreactors or in fenced areas in the field margins to achieve maximum concentration of biodestructors and control their survival. These results will help to improve in practice the process of destruction of rice straw and increase the attractiveness of the biodegradation method compared to the burning of crop residues now practiced. As one of the fundamental results of the project, it was possible to show that in agro-ecosystems at the local level, the composition of communities of soil macroarthropods is primarily determined by local environmental factors and edaphic conditions, while at the regional level, the formation of taxonomic composition of communities is determined by climate and physical-geographical parameters (https: //doi.org/10.1016/j.soilbio.2018.12.002). An additional scientific result was description of six new species for science found during the field work on the project. In 2018, six articles were published or accepted for publication. In fact, additional four manuscripts have already been submitted and are at various stages of review and revision process. Thus, the total number of publications on the project will be at least 12 and include at least four articles in Q1 journals. Given the increased interest in project results in Russia, China and other countries of the Asia-Pacific region, the project results were reported at three All-Russian and one international conference (the Russian-Chinese conference inviting scientists from other countries on "Ecological restoration and sustainable development" 1 July 3, 2018, Changchun, PRC). At the conference it was agreed to continue work on the topic within a multinational project on the rice straw degradation by soil fauna. The project proposal is already drafted and being prepared for submission to the respective funding agencies.

Publications

1. Degtyarev M.I., Korobushkin D.I., Gongalsky K.B., Zaitsev A.S. Население энхитреид (Annelida, Clitellata, Enchytraeidae) и его зависимость от эдафических условий в рисовых агроэкосистемах России Экология, - (year - 2019)

2. Gongalsky K.B., Turbanov I.S., Medvedev D.A., Volkova J.S. Description of a new species of the genus Protracheoniscus Verhoeff, 1917 and redescription of Protracheoniscus kryszanovskii Borutzky, 1957 from the southeast of European Russia (Isopoda, Oniscidea, Agnaridae) ZooKeys, 801: 189–205 (year - 2018) https://doi.org/10.3897/zookeys.801.23167

3. Guo Y., Gao M., Liu J., Zaitsev A.S., Wu D. Disentangling the drivers of ground-dwelling macro-arthropod metacommunity structure at two different spatial scales Soil Biology and Biochemistry, 130: 55–62 (year - 2019) https://doi.org/10.1016/j.soilbio.2018.12.002

4. Kolesnikov V.B., Turbanov I.S., Gongalsky K.B. Two new species of false scorpion genus Ephippiochthonius Beier, 1930 (Arachnida: Pseudoscorpiones: Chthoniidae) from Western Ciscaucasia, Russia. Arthropoda Selecta, - (year - 2019)

5. Ryabinin N.A., Zaitsev A.S. Новые виды панцирных клещей (Acari, Oribatida) с острова Сахалин Зоологический журнал, - (year - 2019)

6. Zaitsev A.S., Gorbunova A.Yu., Korobushkin D.I., Degtyarev M.I., Zhadova A.N., Kostina N.V., Gongalsky K.B. The earthworm species Eisenia fetida modulates greenhouse gas release and carbon stabilization after rice straw amendment to a paddy soil European Journal of Soil Biology, 89:39-44 (year - 2018) https://doi.org/10.1016/j.ejsobi.2018.10.003

7. Gorbunova A.Yu., Korobushkin D.I., Degtyarev M.I., Kostina N.V., Gongalsky K.B., Lebedev Yu.M., Zaitsev A.S. Влияние дождевых червей на эмиссию CO2 и CH4 при разложении рисовой соломы в почвах разных типов при разном уровне влажности Наземные и морские экосистемы Причерноморья и их охрана. Сборник тезисов научно-практической конференции . Новороссийск, Краснодарский край,Россия 23-27 апреля 2018 г., с. 32-33. (year - 2018)

8. Gorbunova A.Yu., Zaytsev A.S., Korobushkin D.I., Degtyarev M.I., Kostina N.V., Gongalsky K.B. Влияние дождевых червей на эмиссию СО2 и СН4 и стабилизацию углерода в почве при разложении рисовой соломы XVIII Всероссийское совещание по почвенной зоологии. 22–26 октября 2018 г., Москва, ИПЭЭ РАН. Материалы докладов. Тов-во научн. изданий КМК, с.65-66 (year - 2018)

9. Korobushkin D.I., Gongalsky K.B., Gorbunova A.Yu., Zaytsev A.S. Почвенная макрофауна рисовых чеков XVIII Всероссийское совещание по почвенной зоологии. 22–26 октября 2018 г., Москва, ИПЭЭ РАН. Материалы докладов. Тов-во научн. изданий КМК,, с.106-107 (year - 2018)

10. Korobushkin D.I., Zaitsev A.S., Saifutdinov R.A., Zaitsev A.S. Cообщества почвенных нематод рисовых агроэкосистем России Сборник материалов V научно-практической молодежной конференции «ЭКОБИО – 2018» 8 – 11 октября 2018 года, г. Севастополь, стр. 27 (year - 2018)

11. Saifutdinov R.A., Zaytsev A.S. Таксоцены коллембол (Hexapoda: Collembola) в рисовых агроэкосистемах России XVIII Всероссийское совещание по почвенной зоологии. 22–26 октября 2018 г., Москва, ИПЭЭ РАН. Материалы докла- дов. Тов-во научн. изданий КМК, с.173-174 (year - 2018)

12. Zaitsev A.S. Почвенные клещи на рисовых чеках: биоиндикационное значение и экосистемные функции. Наземные и морские экосистемы Причерноморья и их охрана. Сборник тезисов научно-практической конференции . Новороссийск, Краснодарский край,Россия 23-27 апреля 2018 г., с.46-47 (year - 2018)

Annotation of the results obtained in 2016
The project “Role of invertebrates in the reduction of greenhouse gas emissions and increase of climatic and environmental safety of rice production in Russia” aimed at solving actual problems of reducing anthropogenic stress on the environment and climate in the rice-growing areas. This is achieved by applying soil animals for maintaining natural soil fertility, biodegradation of rice crop residues and stabilizing carbon and nitrogen in rice soils. In 2016 we collected and analyzed literature data on the fauna and population of soil organisms in the rice paddies. Overall more than 100 literature sources were examined. We found that soil animal communities in the rice paddies are very poor in comparison with the other open habitats at the same latitude. Along with this, its faunistic composition was to the large extent determined by the nature of crop rotation and the period of rice paddies being drained. The dominants composition in such communities is very simple and is characterized by the prevalence of different worm groups, and Enchytraeidae in particular. Few references cover non-tropical areas, including Krasnodar Krai and China. Many authors highlight the importance of volume of fertilizer application in determining biological diversity and functioning of soil communities in the rice paddies. Among most functionally important groups of soil animals, which may stabilize carbon from the rice straw we might note earthworms (from Lumbricidae and Megascolecidae families), different species of Enchytraeidae and to the smaller extent saprotrophic dipteran and coleopteran larvae and diplopods in Krasnodar Krai and hemipterans in the other regions. In the future we are planning to run laboratory experiments with these taxa. We performed field studies at 44 locations in the rice-growing parts of Krasnodar and Primorsky Krais and in the republic of Kalmykia. Field data basically confirmed literature search data. In is notable that the abundance and diversity of different soil taxa was strongly dependent on the type of crop rotation. Typically soil-dwelling taxa belonging to meso- and macrofauna (oribatid mites, springtails, different macrofauna taxa) were more diverse in the non-regularly inundated paddies. In the opposite case enchytraeids clearly dominated. We noted particularly high diversity of the latter group in the rice paddies of Primorsky Krai, what might be explained by the specific biogeographic situation in this territory and less intense land use levels practiced at the Russian Far East. The preliminary results of the pilot laboratory microcosm experiment in the brand-new set of microcosms bring some evidence on the high efficiency of earthworms and carbon stabilizers. Same is potentially applicable for nitrogen after straw application in the rice paddy soil. At the high density of earthworms methane emission from the paddies was considerably reduced. Thi sis important as methane has a very high Global Warming Potential. Most probably, this happens due to stimulating effect of earthworms on the activity of methanotrophic bacteria and in opposite, inhibiting effect on methanogenic bacteria. The project progress is also disclosed in the news section of the Primorsky Institute for Agriculture (http://primnii.ru/index.php/ct-menu-item-7/36-novosti, news in Russian as on 19.09.2016).

Publications

1. - 19 сентября 2016 г. состоялась встреча ученых Института проблем экологии и эволюции им. А.Н. Северцова Российской академии наук и Приморского научно-исследовательского института сельского хозяйства. Новостная лента ПРИМНИИ СХ, http://primnii.ru/index.php/ct-menu-item-7/36-novosti, новость от 19.09.2016 (year - )

Annotation of the results obtained in 2017
The work on all planned laboratory experiments on the estimation of the potential of rice straw degradation and carbon stabilization in the rice paddies by soil animals was competed during the reporting period. We estimated that the most efficient destructors of rice crop residues are earthworms which in the conditions of optimal density (about 530 individuals per square meter) and soil moisture (25% of the water holding capacity) may in the short-term perspective increase carbon content in soil by 1.8%. At the same time the gross potential of carbon immobilization at the national level in Russia with this technique may be up to 4.3 billion tons. We also demonstrated that woodlice Armadillidium vulgare and Protracheoniscus kryszanovskii as well as myriapods Brachydesmus assimilis and Cylindroiulus sp. Maybe also used for rice straw recycling as secondary assistants. The results on the possibility of microbial respiration inhibition by enchytraeids are also very interesting. Although, these worms do not directly degrade straw, in combination with earthworms which are most active during the drained stages of the rice crop rotation in the conditions of Russia, soil inoculation with enchytraeids during the flooded stage of rice growing may help to reduce greenhouse gas emissions and thus improve bulk carbon sequestration balance for the entire crop rotation cycle. We also established the field experiment in the rice paddies in the Republic of Kalmykia and Krasnodarsky Krai. We selected six rice paddies (three in each region) all at the stage of the cover crop. In each of them currently six mesocosms inoculated with Eisenia fetida earthworms are maintained. According to the workplan first scientific results of this experiment are expected in spring 2018. The results of the project were presented at the 10th International Symposium on Terrestrial Isopod Biology in august 2017 in Budapest and in China in October 2017 at the specialized preparatory GSBI roundtable of agroecologists in Changchun. In cooperation with Prof. D. Wu from the North-Eastern Institute of Geography and Agroecology, Chinese Academy of Sciences the application on international scientific cooperation support has been drafted to upscale the results of the current project and study rice straw degradation potential by soil fauna in the entire Asian-Pacific Region. The wide discussion of the results achieved so far had been with the professional agronomists had been organized. Two papers have been published at the Web of Science Journals (https://doi.org/10.11646/zootaxa.4347.3.10; https://doi.org/10.11646/zootaxa.4318.3.11). Two more paper manuscripts were submitted for publication with the description of the new species of woodlice and oribatid mites (to Zootaxa). Four more manuscripts were prepared from the submission to the Web of Science Journals. Thus, the total amount of prepared and published papers is eight what corresponds to the respective reporting benchmark of the Project.

Publications

1. Gongalsky K.B. The first record of the genus Desertoniscus Verhoeff, 1930 (Isopoda, Oniscidea, Agnaridae) from Europe, with the description of a new species Zootaxa, Vol. 4347, No 3, pp. 583–591 (year - 2017) https://doi.org/10.11646/zootaxa.4347.3.10

2. Tanasevich A.V. A new Oreonetides Strand, 1901 from the Russian Far East (Araneae, Linyphiidae) Zootaxa, Vol. 4318, No.3, pp.596–599 (year - 2017) https://doi.org/10.11646/zootaxa.4318.3.11

3. K.B. Gongalsky, P.S. Nefediev, I.S. Turbanov, V.Yu. Slatina, Yu.M. Lebedev Terrestrial isopods (Isopoda, Oniscidea, Agnaridae) from the northernmost limit of isopod distribution in southern Siberia, Russia Abstract Book of the 10th International Symposium on Terrestrial Isopod Biology, P. 26-27 (year - 2017)

4. Korobushkin D.I., Gongalsky K.B. Isotopes in Isopodes: Analyzing ecology of woodlice by using stable isotopes of carbon and nitrogen Abstract Book of the 10th International Symposium on Terrestrial Isopod Biology, P. 35-36 (year - 2017)