- DOI 10.31509/2658-607x-2020-3-2-1-20
- УДК 592:574.42
Impact of earthworms of different morpho-ecological groups on carbon accumulation in forest soils
A.P. Geraskina
Center for Forest Ecology and Productivity of the Russian Academy of Sciences
Profsoyuznaya st. 84/32 bldg. 14, Moscow, 117997, Russia
*E-mail: angersgma@gmail.com
Received 25.05.2020
Accepted 24.06.2020
To date, forest ecology has not made any clear conclusions regarding the impact of large invertebrate saprophages such as earthworms on soil carbon dynamics. Some authors state that earthworm activities result in decreased carbon accumulation. Other studies show that earthworms contribute to soil carbon accumulation. At the same time, many studies do not take into account the differences between trophic and digging activity of different morpho-ecological groups of earthworms in different soil horizons. The objective of this study was to carry out differentiated assessment of the impact of different morpho-ecological groups of earthworms on carbon accumulation and correspondent soil parameters (nitrogen content and С/N ratio) during the change in forest succession status. Field operations were performed in the spring and summer of 2016 and 2018 in three regions: Bryansk Oblast (Bryansk Polesie), Moscow Oblast (Moskva–Oka plain, Valuyevsky urban forest) and Northwest Caucasus (Krasnodar Krai, Apsheron forestry; Republic of Adygeya, Caucasian biosphere reserve). In each region, three main stages of coniferous-broad-leaved forest restoration after clear cuttings were identified. Three test plots 50х50 m were allocated for each stage; geobotanical and soil descriptions as well as earthworm calculations were carried out on each plot. It was found out that during the change in forest succession status the species composition and the set of morpho-ecological groups of earthworms became more complicated, but there was no successive replacement of any groups with others. Negative correlation was found between the total biomass of earthworms feeding on the soil surface (epigeic, epi-endogeic and anecic species) and litter store. In the litter horizon, the biomass of epi-endogeic species was negatively correlated with the content of organic carbon and C/N ratio, but positively correlated with the nitrogen content; in the humus horizon, it was positively correlated with the content of organic carbon and nitrogen and negatively correlated with the С/N ratio. Significant negative correlations were revealed between the biomass of endogeic earthworm species and C/N ratio in the humus horizon.
Key words: forest type, succession status, chronoseries, litter, nitrogen, C/N ratio, invertebrates-saprophages, biomass
REFERENCES
Abaturov B.D., Pochvoobrazujushhaja rol’ zhivotnyh v biosfere (Soil-forming role of animals in the biosphere), Biosfera i pochvy, Moscow: Nauka, 1976. pp. 53-69.
Alban D.H., Berry E.C., Effects of earthworm invasion on morphology, carbon, and nitrogen of a forest soil, Appl. Soil Ecol., 1994, Vol. 1, pp. 243-249.
Andriuzzi W.S., Schmidt O., Brussaard L., Faber J.H., Bolger T., Earthworm functional traits and interspecific interactions affect plant nitrogen acquisition and primary production, Applied Soil Ecology, 2016, Vol. 104, pp. 148-156.
Angst S., Mueller C.W., Cajthaml T., Angst G., Lhotakova Z., Bartuska M., Spaldonova A., Frouz J., Stabilization of soil organic matter by earthworms is connected with physical protection rather than with chemical changes of organic matter, Geoderma, 2017, Vol. 289, pp. 29-35.
Begon M., Harper J.L., Townsend C.R., Ecology: Individuals, Populations and Communities. Oxford: Blackwell Scientifi c Publications, 1986, 1068 p.
Berezina O.G., Struktura naselenija kollembol (Hexapoda, Collembola) reliktovogo lipovogo lesa (Gornaja Shorija, Kemerovskaja oblast’) (The spatial structure of springtails community (Hexapoda, Collembola) of the southern forest-steppe of Western Siberia), Evraziatskij jentomologicheskij zhurnal, 2016, Vol. 15, No 6, pp. 583-590.
Bitjuckij N.P., Solov’eva A.N., Lukina E.I., Olejnik A.S., Zavgorodnjaja Ju.A., Demin V.V., Byzov B.A., Jekskrety dozhdevyh chervej stimuljator mineralizacii soedinenij azota v pochve (Stimulating Effect of Earthworm Excreta on the Mineralization of Nitrogen Compounds in Soil), Pochvovedenie, 2007, No 4, pp. 468-473.
Bohlen P.J., Pelletier D.M., Groffman P.M., Fahey T.J., Fisk M.C., Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests, Ecosystems, 2004, Vol. 7, pp. 13-27.
Burtelow A.E., Bohlen P.J., Groffman P.M., Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States, Appl. Soil Ecol., 1998, Vol. 9, pp. 197-202.
Curry J.P., Factors affecting the abundance of earthworms in soils. In: Edwards C.A. (Ed.). Earthworm Ecology, 2nd ed., CRC Press, Boca Raton, FL, 1994, pp. 91-113.
Frouz J., Liveckova M., Albrechtoa J., Chronakova A., Cajthaml T., … & Simackova H. Is the effect of trees on soil properties mediated by soil fauna? A case study from post-mining sites, Forest Ecology and Management, 2013, Vol. 309, pp. 87-95.
Geras’kina A.P., Preobrazovanija kompleksa dozhdevyh chervej v hode poslerubochnyh sukcescij v lesah Severo-Zapadnogo Kavkaza (Transformations of earthworm communities during post-logging successions in the forests of the Northwest Caucasus), Forest science issues, 2018, No 1, pp. 1-14.
Gilyarov M.S., Metody pochvenno-zoologicheskih issledovanij (Methods of soil and zoological research), Moscow: Nauka, 1975, 304 p.
Gleixner G., Soil organic matter dynamics: a biological perspective derived from the use of compound-specific isotopes studies, Ecological Research, 2013, Vol. 28, No 5, pp. 683-695.
Goncharov A.A., Struktura troficheskih nish v soobshhestvah pochvennyh bespozvonochnyh (mezofauna) lesnyh jekosistem (The structure of trophic niches in the communities of soil invertebrates (mesofauna) of forest ecosystems. Candidate’s biol. sci. thesis), Moscow: IPJeJe, 2014, 177 p.
Hirth J.R., Li G.D., Chan K.Y., Cullis B.R., Long-term effects of lime on earthworm abundance and biomass in an acidic soil on the south-western slopes of New South Wales, Australia, Applied Soil Ecology, 2009, Vol. 43, pp. 106-114.
Hoeffner K., Monard C., Santonja M., Cluzeau D., Feeding behaviour of epi-anecic earthworm species and their impacts on soil microbial communities, Soil Biology and Biochemistry, 2018, Vol. 125, pp. 1-9.
Holdsworth A.R., Frelich L.E., Reich P.B., Leaf litter disappearance in earthworm-invaded northern hardwood forests: role of tree species and the chemistry and diversity of litter, Ecosystems, 2012, Vol. 15, No 6, pp. 913-926.
Huang W., Gonzalez G., Zou X., Earthworm abundance and functional group diversity regulate plant litter decay and soil organic carbon level: A global meta-analysis, Applied Soil Ecology, 2020, Vol. 150, pp. 1-15.
Klassifikacija i diagnostika pochv Rossii (Classification and diagnostics of Russian soils), Shishov L.L., Tonkonogov V.D., Lebedeva I.I., Gerasimova M.I. (Compl.), Smolensk: Ojkumena, 2004, 342 p.
Kozlovskaja L.S., Archegova I.B., Rakova H.N., Biohimicheskoe vozdejstvie pochvennyh bespozvonochnyh na rastitel’nye ostatki (Biochemical effects of soil invertebrates on plant debris), Bolotnye biogeocenozy i ih izmenenija v rezul’tate antropogennogo vozdejstvija, Leningrad: Nauka, 1983, pp. 24-26.
Kozlovskaja L.S., Rol’ pochvennyh bespozvonochnyh v transformacii organicheskogo veshhestva bolotnyh pochv (The role of soil invertebrates in the transformation of organic matter of bog soils), Leningrad, 1976, 211 p.
Kuznecova A.I., Lukina N.V., Tihonova E.V., Gornov A.V., Gornova M.V., Smirnov V.E., Geras’kina A.P., Shevchenko N.E., Teben’kova D.N., Chumachenko S.I., Akkumulyaciya ugleroda v peschanyh i suglinistyh pochvah ravninnyh hvojno-shirokolistvennyh lesov v hode poslerubochnyh vosstanovitel’nyh sukcessij (Сarbon stock in sandy and loamy soil of coniferous-deciduous forestsat the different stages of successions), Pochvovedenie, 2019, No 7, pp. 803-816.
Lavelle P., Martin A., Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics, Soil Biology and Biochemistry, 1992, Vol. 24, No. 12, pp. 1491-1498.
Lavelle P., Pashanasi B., Charpentier F., Gilot C., Rossi J.-P., …& Bernier N., Large- scale effects of earthworms on soil oranic matter and nutrient dynamics, Edwards C.A. (Ed.), Earthworm ecology, St. Lucie Press, 1998, pp.103-122.
Lee K.E., Earthworms. Their ecology and relationships with soils and land use, Academic Press, 1985, 411 p.
Lukina N.V., Tihonova E.V., Shevchenko N.E., Gornov A.V., Kuznecova A.I., … & Shanin V.N., Akkumuljacija ugleroda v lesnyh pochvah i sukcessionnyj status lesov (Carbon accumulation in forest soils and forest succession status), N.V. Lukinа (Ed.), Moscow: KMK, 2018, 232 p.
Makeschin F., Earthworms (Lumbricidae: Oligochaeta): Important promoters of soil development and soil fertility, G. Benckiser (Ed.), Fauna in soil ecosystems. Recycling processes, nutrient fluxes and agricultural production, Florida: CRC Press, 1997, pp. 173-223.
McDaniel J.P., Stromberger M.E., Barbarick K.A., Cranshaw W., Survival of Aporrectodea caliginosa and its effects on nutrient availability in biosolids amended soil, Applied soil ecology, 2013, Vol. 71, pp. 1-6.
Mengel K., Turnover of organic nitrogen in soils and its availability to crops, Plant and Soil, 1996, Vol. 181, pp. 83-96.
Metodicheskie ukazanija po kolichestvennomu opredeleniju obema pogloshhenija parnikovyh gazov (Guidelines for the quantification of greenhouse gas absorption), Rasporjazhenie Minprirody Rossii 30.06.2017, No 20-r, 108 p.
Moore J.-D., Ouimet R., Bohlen P.J., Effects of liming on survival and reproduction of two potentially invasive earthworm species in nothern forest Podzol, Soil Biology and Biochemistry, 2013, Vol. 64, pp. 174-180.
Nacional’nyj atlas pochv Rossijskoj Federacii (National Atlas of Soils of the Russian Federation), Shoba S.A., Aljabina I.O., Urusevskaja I.S., Chernova O.V., Moskow: Astrel’, 2011, 632 p.
Novara A., Rühl J., La Mantia, T., Gristina L., La Bella, S., Tuttolomondo T., Litter contribution to soil organic carbon in the processes of agriculture abandon, Solid Earth, 2015, Vol. 6, No 2, pp. 425-432.
Parmelee R.W., Crossley Jr., Earthworm production and role in the nitrogen cycle of a no-tillage agroecosystem on the Georgia piedmont, Pedobiologia, 1988, Vol. 32, pp. 353-361.
Perel’ T.S., Rasprostranenie i zakonomernosti raspredelenija dozhdevyh chervej fauny SSSR (Distribution and distribution patterns of earthworms of the fauna of the USSR), Moskow: Nauka, 1979, 272 p.
Pulleman M.M., Six J., Uyl A., Marinissen J.C.Y., Jongmans A.G., Earthworms and management affect organic matter incorporation and microaggregate formation in agricultural soils, Appl. Soil Ecol., 2005, Vol. 29, pp. 1-15.
Sandor M., Schrader S., Earthworms affect mineralization of different organic amendments in a microcosm study, Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Agriculture, 2007, Vol. 63, pp. 442-447.
Sariyildiz T., Effects of tree canopy on litter decomposition rates of Abies nordmanniana, Picea orientalis and Pinus sylvestris, Scandinavian journal of forest research, 2008, Vol. 23, No. 4, pp. 330-338.
Sariyildiz T., Küçük M., Litter mass loss rates in deciduous and coniferous trees in Artvin, northeast Turkey: Relationships with litter quality, microclimate, and soil characteristics, Turkish journal of Agriculture and Forestry, 2008, Vol. 32, No. 6, pp. 547-559.
Shevchenko N.E., Kuznecova A.I., Teben’kova D.N., Smirnov V.E., Geras’kina A.P., Gornov A.V., Tihonova E.V., Lukina N.V., Sukcessionnaya dinamika rastitel’nosti i zapasy pochvennogo ugleroda v hvojno-shirokolistvennyh lesah severo-zapadnogo Kavkaza (The succession dynamics of vegetation and carbon stocks in coniferous-deciduous forests of the north-western Caucasus), Lesovedeniе, 2019, No 3, pp. 163-176.
Striganova B.R., Issledovanie roli mokric i dozhdevyh chervej v processah gumifikacii razlagajushhejsja drevesiny (Investigation of the role of woodlice and earthworms in the processes of humification of decaying wood), Pochvovedenie, 1968, №. 8, pp. 85-90.
Striganova B.R., Kozlovskaja L.S., Chernobrovkina N.P., Kudrjasheva I.V., Pishhevaja aktivnost’ dozhdevyh chervej i soderzhanie aminokislot v temnoseroj lesnoj pochve (Alimentative activity of earthworms and content of aminoacids in the dark grey forest soil), Pochvovedenie, 1989, No 5, pp. 44-51.
Striganova B.R., Pitanie pochvennyh saprofagov (Nutrition of soil saprophages), Moskow: Nauka, 1980, 243 p.
Striganova B.R., Sukcessii zhivotnogo naselenija pochvy v processe pervichnogo pochvoobrazovanija (Successions of the animal population of the soil in the process of primary soil formation), Rannjaja kolonizacija sushi, Moskow: PIN RAN, 2012, pp. 177-195.
Suarez E.R., Fahey T.J., Yavitt J.B., Groffman P.M., Bohlen P.J., Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms, Ecological Applications, 2006, Vol. 16, No 1, pp. 154-165.
Talashilkar S.C., Bhangarath P.P., Mehta V.B., Changes in chemical properties during composting of organic residues as influenced by earthworm activity, Journal of the Indian Society of Soil Science, 1999, Vol. 47, pp. 50-53.
Vsevolodova-Perel’ T.S., Dozhdevye chervi fauny Rossii. Kadastr i opredelitel’ (Earthworms of Russia. Cadastr and key-book.), Moskow: Nauka, 1997, 101 p.
Vsevolodova-Perel’ T.S., Gryuntal’ S.Yu., Kudryasheva I.V., Nadtochij S.E., Golovach S.I., Matveeva A.A., Osipov V.V., Karpachevskij L.O., Rastvorova O.G., Struktura i funkcionirovanie pochvennogo naseleniya dubrav Srednerusskoj lesostepi (The structure and functioning of the soil population of the oak forests of the Central Russian forest-steppe). Moscow: Nauka, 1995, 152 p.
World Reference Base for Soil Resources, International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports, IUSS Working Group. Rome: FAO, 2015, 203 р.
Zhukov A.V., Dozhdevye chervi kak komponent biogeocenoza i ih rol’ v zooindikacii (Earthworms as a component of biogeocenosis and their role in zooindication), Ґruntoznavstvo, 2004, Vol. 5, No 1-2, pp. 44-57.
Zhukov A.V., Jekologicheskoe raznoobrazie zhivotnogo naselenija pochv pojmennyh biogeocenozov reki Samara (Ecological diversity of the animal population in the soils of floodplain biogeocenoses of the Samara River), Vіsnik Dnіpropetrovs’kogo unіversitetu. Bіologіja. Ekologіja, 2000, No 7. pp. 73-79.
Zhukovskaja E.A., Kodolova O.P., Pravduhina O.Ju., Varne A.Zh., Boloteckij N.M., Issledovanie geneticheskogo raznoobrazija dozhdevogo chervja Lumbricus rubellus Hoff. (Oligochaeta, Lumbricidae) (Study of genetic diversity of earthworm Lumbricus rubellus Hoff. (Oligochaeta, Lumbricidae), Izvestija Rossijskoj akademii nauk. Serija biologicheskaja, 2005. No 5. pp. 625-627.