IMPACT OF EARTHWORMS OF DIFFERENT MORPHO-ECOLOGICAL GROUPS ON CARBON ACCUMULATION IN FOREST SOILS

Morpho-ecological group	Region	Forest type	Species	Number, ind./m2±SE
Epigeic (4 species)	Bryansk Woodlands	B1	–	–
		B2	D. octaedra	12.0±4.6
			D. r. tenuis	2.0±0.3
		B3	D. octaedra	7.3±2.8
			D. r. tenuis	0.7±0.3
			Total: 2 species
	Moskva–Oka plain	M1	–	–
		M2	D. octaedra	8.8±0.8
			L. castaneus	0.8±0.1
		M3	D. octaedra	6.4±1.3
			D. r. tenuis	2.0±0.5
			L. castaneus	0.9±0.2
			Total: 3 species
	Northwest Caucasus	C1	D. octaedra	1.3±0.2
			D. attemsi	0.3±0.1
		C2	D. octaedra	7.0±1.6
			D. attemsi	0.7±0.3
		C3	D. octaedra	1.7±0.3
			D. attemsi	0.3±0.1
			D. r. tenuis	0.3±0.1
			Total: 3 species
Epi-endogeic (3 species)	Bryansk Woodlands	B1	–	–
		B2	E. nordenskioldi	0.3±0.2
		B3	L. rubellus	1.3±0.4
			Total: 2 species
	Moskva–Oka plain	М1	L. rubellus	14.0±4.5
		M2	L. rubellus	16.0±4.5
		M3	L. rubellus	42.0±7.6
			Total: 1 species
	Northwest Caucasus	C1	E. fetida	0.5±0.06
		C2	–	–
		C3	E. fetida	0.5±0.1
			Total: 1 species
Endogeic (6 species)	Bryansk Woodlands	B1	–	–
		B2	–	–
		B3	–	–
	Moskva–Oka plain	M1	А. c. caliginosa	29.0±4.7
			A. rosea	32.0±5.6
			O. lacteum	4.0±0.5
		M2	А. c. caliginosa	39.2±7.1
			A. rosea	16.0±3.9
		M3	А. c. caliginosa	8.0±2.4
			A. rosea	4.8±0.9
			Total: 3 species
	Northwest Caucasus	C1	A. jassyensis	11.3±3.0
			D. s. schmidti	17.7±2.9
			D. tellermanica	5.7±1.5
		C2	A. jassyensis	6.3±3.5
			D. s. schmidti	22.0±4.8
		C3	A. jassyensis	8.0±1.0
			D. s. schmidti	24.6±8.6
			Total: 3 species
Anecic (3 species)	Bryansk Woodlands	B1	–	–
		B2	–	–
		B3	–	–
	Moskva–Oka plain	M1	–	–
		M2	A. longa	3.2±0.2
			L. terrestris	1.6±0.1
		M3	A. longa	1.6±0.4
			L. terrestris	0.8±0.3
			Total: 2 species
	Northwest Caucasus	C1	D. mariupolienis	0.5±0.3
		C2	D. mariupolienis	2.0±0.2
		C3	D. mariupolienis	6.7±3.3
			Total: 1 species

Morpho-ecological group	Compared forest types	df	Нu	Р
Epigeic	*B2 х B3	1	2.167	0.041**
	M2 х M3	1	0.079	0.777
	C1 х С2 х С3	2	0.492	0.781
Epi-endogeic	B2 x B3	1	1.750	0.048**
	M2 x M2 x M3	2	4.610	0.036**
	C1 x C3	1	0.437	0.508
Endogeic	M2 x M2 x M3	2	8.564	0.014**
	C1 х С2 х С3	2	0.862	0.649
Anecic	M2 х M3	1	0.784	0.375
	C2 x C3	1	4.419	0.012**
All groups	B1 x B2 x B3	2	6.882	0.032**
	M2 x M2 x M3	2	0.929	0.629
	C1 х С2 х С3	2	0.965	0.617

Note: *For designation of forest types B1…C3, see Table 1.

 ** The differences are statistically significant (p≤0.05).

Thus, with changing plant communities and the litter quality becoming more favorable for earthworms, epigeic and epi-endogeic species show themselves in the soils of light granulometric composition of the Bryansk Woodlands. Nevertheless, the number of earthworms remains numerically insignificant, and they do not play any significant functional role in litter decomposition (Lukina et al., 2018).

1.2 Forests of the Moskva–Oka plain

9 species of earthworms belonging to 4 morpho-ecological groups were found: epigeic D. r. tenuis, D. octaedra, Lumbricus castaneus (Savigny, 1826); epi-endogeic L. rubellus, endogeic Aporrectodea caliginosa caliginosa (Savigny, 1826), Aporrectodea rosea (Savigny, 1826), Octolasium lacteum (Oerley, 1885), and anecic Lumbricus terrestris Linnaeus, 1758, Aporrectodea longa (Ude, 1885). Factors favorable for earthworm vital activity in these forests are the granulometric composition of soils (middle loamy), the presence of high-quality litter from trees and shrubs, as well as the optimal litter acidity (5.8–6.1) at all stages of succession.

In birch-linden forests with aspen (M1), 4 species of earthworms were found: the epi-endogeic L. rubellus as well as endogeic A. с. caliginosa, A. rosea, and O. lacteum. Endogeic species make the largest contribution to the biomass (Fig. 1). The absence of epigeic species is probably due to the rapid utilization of high-quality litter of linden and birch by soil biota (Berezina, 2016).

In linden forests with birch and aspen (M2), 7 species of earthworms were identified: epigeic D. octaedra, L. castaneus, epi-endogeic L. rubellus, endogeic A. с. caliginosa, A. rosea, and anecic L. terrestris, A. longa (Table 1). Despite the presence of 4 morpho-ecological groups of Lumbricidae, the biomass of endogeic species exceeds the biomass of earthworms of other groups (Fig. 1).

In broadleaf spruce forests (M3), 8 species of earthworms were identified: epigeic D. octaedra, D. r. tenuis, L. castaneus, epi-endogeic L. rubellus, endogeic A. caliginosa, A. rosea, and anecic L. terrestris, A. longa. The difference between the spruce-broadleaf forest and the two previous stages of the chronoseries is a significant decrease in the biomass of endogeic species and the 4.5-fold increase in the biomass of the epi-endogeic L. rubellus.

Thus, in the middle loamy soils of the Moskva–Oka plain, the completed complex of earthworms is only found in the oldest forests (older than 110 years). Despite the presence of rapidly decomposing broadleaf litter (from linden, birch), only two morpho-ecological groups of earthworms are active in these forests at the initial stages of succession, i.e. endogeic and epi-endogeic. With increasing age of forest communities and increasing proportion of slowly decomposing litter (spruce) in the litter horizon, the conditions for epigeic, epi-endogeic and anecic species that feed on leaf litter of trees, shrubs and herbs on the soil surface remain favorable (Perel’, 1979; Hoeffner et al., 2018; Huang et al., 2020).

1.3 Forests of the Northwest Caucasus

8 species of earthworms belonging to 4 morpho-ecological groups were found: epigeic D. r. tenuis, D. octaedra, Dendrobaena attemsi Michaelsen, 1902; epi-endogeic Eisenia fetida (Savigny, 1826), endogeic Dendrobaena schmidti schmidti (Michaelsen, 1907), Dendrobaena tellermanica Perel’, 1966, Aporrectodea jassyensis (Michaelsen, 1891), and anecic Dendrobaena mariupolienis Wyssotzky, 1898.

7 species of earthworms were found in aspen-hornbeam forests (C1): epigeic D. octaedra, D. attemsi; epi-endogeic E. fetida; endogeic D. s. schmidti, D. tellermanica, A. jassyensis, and anecic D. mariupolienis (Table 1). The biomass of endogeic species is significantly higher than that of other groups (Fig. 1).

5 species of earthworms were found in fir-beech-hornbeam forests (C2): epigeic D. octaedra, D. attemsi; endogeic D. s. schmidti, A. jassyensis, and anecic D. mariupolienis.

In the oldest fir-beech forests (C3), that are older than 400 years, 7 species of earthworms were identified: epigeic D. octaedra, D. attemsi, D. r. tenuis; epi-endogeic E. fetida; endogeic D.s. schmidti, A. jassyensis, and anecic D. mariupolienis. An important feature of the earthworm population at the terminal stage of succession of coniferous-broadleaf forests of the Northwest Caucasus is a 4–9-fold increase in the biomass of anecic earthworms as compared to the previous stages of the chronological order (Geraskina, 2018), the differences are statistically significant (Fig. 1, Table 2).

In general, 4 morpho-ecological groups of earthworms were present in the chronoseries of the forests of the Northwest Caucasus already at the initial stages, which is due to favorable forest brown soils and the presence of mixed litter, which is better for earthworms in trophic and topical terms (Sariyildiz, 2008; Sariyildiz, Küçük, 2008). Litter acidity at all stages of succession is close to optimal values (pH 5.1–6.0) and does not limit the activity of earthworms. As in the forests of the Moskva–Oka plain, increasing biomass of anecic earthworms was observed in the Northwest Caucasus in the process of succession.

Thus, the example of three types of forest study objects in different regions showed that the set of morpho-ecological groups of earthworms is determined by the soil granulometric composition and litter quality of the tree layer, undergrowth and shrubs. At the initial stages of post-cutting forest restoration, the composition of morpho-ecological groups of earthworms is incomplete (with the exception of the forests of the Northwest Caucasus). With changing succession status of forests, the set of morpho-ecological groups of earthworms becomes more complex, but there is no successive replacement of one group by others.

2. Impact of earthworms of different morpho-ecological groups on carbon accumulation in forest soils and associated soil parameters, such as litter store, nitrogen content, and C/N ratio

Litter thickness relies on the activity of earthworms (Vsevolodova-Perel’ et al., 1995; Suarez et al., 2006; Holdsworth et al., 2012; Huang et al., 2020, etc.). Correlation analysis showed that in all regions, the stock of the L subhorizon is negatively related to the biomass of earthworms active in the litter horizon. The highest values of the coefficient of determination (R² = 0.65) were obtained for the forests of the Bryansk Woodlands, where the store of L subhorizon is at least twice as high as compared to the forests of the Moskva–Oka plain and the Northwest Caucasus (with the exception of plots of old-aged fir-beech forests) (Fig. 2). Litter accumulation in the forests of the Bryansk Woodlands corresponds to a very low biomass of earthworms (Fig. 1). As our studies have shown, the biomass of other groups of saprophagous invertebrates is also small here. Litter store in the forests of the Moskva–Oka plain is probably more actively controlled by the activity of the epi-endogeic L. rubellus, since its contribution to the total biomass of earthworms is significantly higher in most forest communities than the contribution of epigeic and anecic species (Fig. 1).

In the forests of the Northwest Caucasus, among the groups of earthworms that regulate litter stores, anecic species make the greatest contribution due to their significantly higher biomass than that of epigeic and epi-endogeic species (Fig. 1).

A significant negative correlation was found between the biomass of epi-endogeic earthworms and the C/N ratio in the litter and in the humus horizon (the example of the forests of the Moskva–Oka plain, where the highest biomass of L. rubellus was found (Fig. 3a, 4a)). And on the contrary, the biomass of epi-endogeic L. rubellus is positively related to the nitrogen content in the litter and the humus horizon (Fig. 3b, 4b). At the same time, the direction of correlation with the organic carbon content differs: a negative correlation of carbon content with the biomass of epi-endogeic earthworms is shown in the litter L subhorizon (Fig. 3c), whereas in the humus horizon, on the contrary, there is a positive correlation (Fig. 4c). Since epi-endogeic earthworms actively feed on the soil surface, which can lead to a decrease in the organic carbon content in the litter, but at the same time they belong to the primary humus-forming agents (Perel’, 1979), it is most likely that the effect of organic matter accumulation during humus formation is more pronounced in the humus horizon. In addition, as a result of motor activity, organic carbon is transferred from the litter horizon to the humus horizon.

Significant correlations of the biomass of endogeic species were found only with the C/N ratio in A horizon (Fig. 5), where earthworms of this group are most active provided the humidity is sufficient. No significant correlations of endogeic species with nitrogen and carbon content were established.

 

The lack of mineral forms of nitrogen is one of the crucial limiting factors of plant mineral nutrition, since up to 90% of this element in soils is in the form inaccessible to plants (Mengel, 1996). The activity of earthworms is known to result in soil enrichment with nitrogen forms available for plants. Earthworm coprolites are rich with urea and ammonium ions. Digestive enzymes of earthworms boost the activity of nitrifying and ammonifying bacteria thus reducing the loss of free nitrogen, which is fixed in the form of compounds, ammonium nitrogen going into nitrites and nitrates (Kozlovskaja, 1976). Experiments with Eisenia nordenskioldi, which live in dark gray soil under broadleaf forests, have shown that the soil is enriched with active forms of amino nitrogen available for absorption by plant roots, as well as with free and bound amino acids (Kozlovskaja et al., 1983; Striganova et al., 1989). In experiments with epi-endogeic and endogeic earthworms it was shown that ammonium contained in earthworm coprolites is able to modify soil nitrification, causing long-term cumulative effects that are vastly superior to their direct effect (Bitjuckij et al., 2007). In experiments with anecic earthworms, it was shown that the available nitrogen content in the soil increased by 0.03 mg/kg for every 0.1 g of earthworm biomass (Andriuzzi et al., 2016). In natural ecosystems, the flow of soil nitrogen through earthworm populations amounts to dozens of kilograms per hectare per year (Lee, 1985; Parmelee and Crossley, 1988), which is necessary for the sustainable functioning of terrestrial ecosystems. Also, the soil is enriched with nitrogen through the death of earthworms: their annual mortality rate is on average 60% of the total population (Lavelle et al., 1998). In the soils of Central Europe, the nitrogen yield reaches 24 g/m² after the death of earthworms, which is comparable to the annual dose of mineral nitrogen fertilizers (100–200 kg of N per 1 ha). Earthworm biomass containing 65–75% of protein decomposes quickly in the soil, but nitrogen bound by microorganisms is washed out more slowly (Lee, 1985; Makeschin, 1997; et al.).

Earthworms contribute to a significant decrease in the C/N ratio in the soil due to their direct and indirect influence on the mineralization and humification of organic matter. Thanks to earthworms there is a three-fold decrease in the C/N ratio in the soil as compared to the litter fall (Striganova, 1968). There is experimental evidence of a significant decrease of the C/N ratio under the influence of different morpho-ecological groups of earthworms not only in forest soils. For epi-endogeic earthworms, this has been shown in vermicompost (Talashilkar et al., 1999), and for endogeic earthworms – in agricultural fields (Sandor, Schrader 2007; McDaniel et al. 2013).

Earthworms are more often classified as nitroliberants, i.e. soil organisms that have a strong influence on nitrogen migration (Kozlovskaja, 1976; Zhukov et al., 2000), primarily due to the humification of organic matter in the soil. However, earthworms as primary litter decomposers and secondary decomposers of dead plant residues also affect the migration of carbon in soils, so they can also be attributed to the group of carboliberants (mineralizing agents). According to our and literature data, the influence of different morpho-ecological groups of earthworms on the nitrogen content and the C/N ratio is similar in the horizons of their activity: the nitrogen content increases, the C/N ratio decreases. However, a differential functional approach is required in regard to the effect of earthworms on carbon content. The latest global meta-analysis shows that the presence of not only epigeic and anecic groups, but also of endogeic earthworms leads to a decrease in organic matter in the litter horizon, with the strongest effect being exerted by anecic earthworms (Huang et al., 2020).

Our study shows a possible significant negative effect of the group of epi-endogeic earthworms (L. rubellus) on litter store and the content of organic carbon in it. It is known that this species is often confined to rich soils and a high content of organic matter (Zhukov, 2004; Zhukovskaja et al., 2005, etc.). We have identified the relationship between the biomass of the epi-endogeic L. rubellus and increased carbon content in the humus horizon. This is probably due to the high trophic activity of these earthworms and high quality of rapidly decomposing litter fall (birch, linden, hazel). No significant correlations between the biomass of endogeic species and the level of carbon accumulation were revealed, but there is a general trend towards decreased organic carbon content in the humus horizon with an increase in the biomass of this group of species. Endogeic species feed on humus (Perel’, 1979; Zhukov, 2004); their coprolites show a decrease in the total mass of organic matter and an increase in ash content by 2–3% as compared to the soil (Lavelle, Martin, 1992; Angst et al., 2017). Endogeic species are not involved in active movement of litter and transfer of organic carbon to the underlying horizons. To obtain convincing results, more field experiments in forest soils are needed, and we intend to continue our research in this area. 

CONCLUSIONS:

1. With the change in the succession status of forests, the species composition and the set of morpho-ecological groups of earthworms become more complex, but there is no consistent replacement of any one group by others.
2. The species richness, diversity of morpho-ecological groups, and biomass of earthworms with similar granulometric composition of soils is determined by the litter quality: the most favorable type of litter fall for maintaining the functional diversity of earthworms is the mixed litter of broadleaf and coniferous species of the tree canopy, undergrowth, and shrubs.
3. Ambiguous effects of earthworms of different morpho-ecological groups on carbon accumulation in forest soils were revealed. Negative correlations were found between the total biomass of epigeic, epi-endogeic, and anecic earthworm species and the litter carbon content. In the humus horizon, the biomass of epi-endogeic species was positively correlated with the carbon content. This study revealed no relationship between the carbon content of the soil and the earthworm anecic species.
4. Indicators associated with carbon accumulation, i.e. the C/N ratio and the nitrogen content, show similar (unidirectional) correlations with the biomass of earthworms in the horizons of their activity: with an increase in the biomass of earthworms of different morpho-ecological groups, the C/N ratio decreases, whereas the nitrogen content increases.

ACKNOWLEDGEMENTS

The study was conducted within the framework of the state CEPF RAS assignment AAAA-A18-118052590019-7, the material was obtained using the grant of the Russian Science Foundation (project No. 16-17-10284).

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Reviewer: candidate of Biological Sciences, Senior Research Officer Zenkova I.V.