Summary

UNIVERSITY OF LATVIA
FACULTY OF GEOGRAPHY AND EARTH SCIENCES
DEPARTMENT OF ENVIRONMENTAL SCIENCES
Jānis Ventiņš
CHANGES OF EARTHWORM (OLIGOCHAETA,
LUMBRICIDAE) COMMUNITIES BY INTERACTION OF
NATURAL AND ANTHROPOGENIC FACTORS
Summary of Thesis for Doctor’s Degree in Environmental Sciences
Riga 2011

The research was carried out at the Institute of Biology of the University of Latvia and
Department of Environmental Sciences at the Faculty of Geography and Earth Sciences
of University of Latvia. The European Social Fund project “Research support for PhD
students and young scientists at the University of Latvia” ensured the financial support
during the development of the research.
Scientific supervisor
Dr. Biol. Viesturs Melecis
Doctoral committee
Council
Reviewers
The defence of the doctoral thesis will be held on
The thesis is available at the Library of the University of Latvia, 4 Kalpaka Blvd
2

CONTENTS
CONTENTS ................................................................................................................................................3
INTRODUCTION ......................................................................................................................................4
1. EARTHWORMS IN AGRICULTURAL LANDS...............................................................................9
1.1. EARTHWORM IMPACT ON SOIL PROPERTIES AND MICROORGANISMS...........................................11
1.2. EARTHWORMS AND SOIL CULTIVATION......................................................................................... 12
1.3. EARTHWORM IMPACT ON GRICULTURAL LAND QUALITY BIOINDICATION................................... 13
2. THE MONITORING SYSTEM OF AGRICULTURAL LANDS....................................................14
2.1. DESCRIPTIOM OF THE MONITORING SAMPLING PLOTS ................................................................ 14
2.2. FACTORS EFFECTING EARTHWORM DENSITY AND COMMUNITY STRUCTURE IN THE MONITORING
SAMPLING PLOTS .................................................................................................................................. 15
3. CHANGES OF EARTHWORM COMMUNITIES IN ACIDIC PINE FOREST SOILS ..............19
3.1. LATVIA’S OLIGOTROPHIC FOREST SOIL EARTHWORM FAUNA IN LATVIA AND NORTHERN EUROPE
.............................................................................................................................................................. 19
3.2. EARTHWORM FAUNA CHANGES DUE TO FOREST LIMING.............................................................. 21
3.3. LATVIA’S BOREAL PINE FOREST EUTROPHICATION AND TRANSFORMATION ............................... 22
3.4. EARTHWORM SPECIES COMMUNITIES CHANGES DUE TO TRANSFORMATION OF JURMALA
FOREST SOILS........................................................................................................................................ 23
3.4.1. Description of the sampling plots and sampling procedure ................................................... 23
3.4.2. The total earthworm population density in Jurmala sampling plots ...................................... 25
3.4.3. Soil property change impact on earthworm communities ...................................................... 26
3.4.4. Earthworm communities structure in Jurmala sampling plots............................................... 27
3.5. EARTHWORM COMMUNITIES CHANGE DUE TO THE INDUSTRIAL POLLUTION IN THE PINE
FORESTS NEAR SAULKALNE ................................................................................................................. 29
3.5.1. Description of the sampling plots and sampling procedure ................................................... 29
3.5.2. The total earthworm population in Saulkalne sampling plots................................................ 31
3.5.3. Pollution impact on the earthworm populations .................................................................... 34
3.5.4. The earthworm communities structure in Saulkalne sampling plots ...................................... 34
3.6. THE POTENTIAL EARTHWORM IMPACT ON PROCESSES OF SOIL EUTROPHICATION IN THE
FORESTS OF JURMALA AND SAULKALNE ............................................................................................. 36
3.7. ROLE OF EARTHWORMS IN THE BIOINDICATION OF THE PINE FOREST EUTROPHICATION
PROCESSES............................................................................................................................................ 37
CONCLUSIONS.......................................................................................................................................39
LITERATURE..........................................................................................................................................41
3

INTRODUCTION
Earthworms are considered as one of the most important biotic components of the soil.
They participate in mineralization and breakdow of organic matter, in formation of the
soil structure and humus, thus providing maintenance of the soil fertility. The significant
importance of earthworms in these processes was emphasized already by C.Darwin
(Darwin, 1881). During the course of several years earthworms may process all the
surface of the soil through their digestive systems. In the intestinal tract of earthworms
forms the so-called caprolite - a well structured mass of the soil and organic waste. In
comparision with the surrounding soil, the casts are less acid, more humid, and they are
richer in nutrients available to plants and microorganisms. Casts significantly improve
physical and chemical properties of the soil.
Earthworms is one of the most investigated animal groups in the world (Lee,
1985), however many of the functional aspects related to the earthworm activity are
still uncertain. Lately, increases researcher interest on the effects of earthworm
activities- both on the soil processes and in level of the ecosystem (Frelich et al.,
2006; Coûteaux, Bolger, 2000). Earthworms are often reffered to as „engineers of the
ecosystems” (Lee, 1985). Earthworms are sensitive to different agrotechnical and
forestry acitvities, as well as to the anthropogenic pollution. They are an appropriate
soil quality change bioindicator, as they are relatively less sensitive to the influence
of different natural external factors (Christensen et al., 1987; Paoletti, 1999).
In Latvia reasearches on earthworms are fragmentary and incomplete. The
most significant researches have been conducted under guidance of V.Eglītis in the
middle of the last century, covering mainly agricultural lands (Эглитис, 1954). In the
seventies nearby Broceni cement plant, M.Šternbergs carried out observations on
lime dust impact on the earthworm populations in natural forest biocommunities
(Штернбергс, 1985). Since the ninties of the last century, the author of the doctoral
paper at Biological institute of University of Latvia has carried out systematic
reasearches on Latvia’s earthworm ecology. Researches have been carried out on the
earthworm species structure and the population dynamic dependency on different
4

environmental factors, as well as on their bioindicative significance. The doctoral
paper includes the author’s reasearch results on the earthworm species communities
changes due to the agrotechnical activities in the most common agricultural soil
varieties, as well as due to the industrial pollution and recreation in transformed pine
forest soils, in all cases having regard to the fluctuations of meteorological factors as
one of the major factors. In reasearches of agricultural communities agricultural soil
monitoring data were used, in obtaining of whom the author took part during the
period from 1992 to 1998. Researches on the effects of industrial pollution were
carried out from 1989 to 1991 near Saulkalne dolomite processing plant. Researches
on the recreation effects on earthworm species communities were carried out in the
territory of Jurmala city from 1989 to 1990.
The objective of the paper: The objective of the doctoral paper is to clarify
the role of earthworms on the soil characterisation against a background of different
antrophogenic factors interaction with natural environmental factors significant to
this organic group, and to assess the bioindicative significance of earthworms.
The tasks of the paper:
- To clarify the structure of earthworm species communities in the most
common agricultural soil varieties;
- To clarify the impact of agricultural activities on the composition of
earthworm species and quantity dynamics in agricultural lands in interaction with
meteorological factors;
- To clarify changes of earthworm species communities and their population
density in pine forest soils transformed by calcium-containing emissions of the
building material factory;
- To clarify changes of earthworm species communities and their population
density in oligotrophic pine forest soils due to the load of permanent recreation;
- To evaluate the indicative significance of different parametres characterizing
earthworm communities structure.
5

The scientific novelty of research
For the first time have been researched the earthworm species compostition
change regularities due to eutrophication of the temperate zone’s oligotrophic pine
forest soils in comparision with forest vegetation changes, and has been assessed the
bioindicative significance of earthworms in assessement of soil eutrophication
processes. Has been researched the specific interaction of agrotechnical activities and
metereological factors on the earthworm population and the species structure in
different varieties of agricultural soils.
For the first time in Latvia have been carried out systematic permanent
researches on forest and agricultural ecosystem earthworm species complex changes
against the background of natural and antrophogenic factors, and has been made
obtained data comparision with other data obtained in other regions of the temperate
zone of Europe. In order to facilitate sustainable agriculture has been clarified the
bioindicative role of the earthworm species complex in assessment of agricultural
soil agrotechnical activity load.
New data have been obtained on the impact of calcium-containing industrial
pollution on changes of the earthworm population and the species structure in acidic
forest soils. Has been formed a hypothesis of earthworms as contributors of soil
physical and chemical changes due to the calcium-containing industrial pollution, as
well as due to the recreational load in the acidic pine forest soils.
Based on the obtained results, have been segregated the earthworm species
communities characteristic to forests of different eutrophication stages and fields of
different cultivation intensity.
During the researches first time in Latvia was found earthworm species
Aporrectodea limicola.
6

Aprobation of te Results
Te results of the thesis are published in 1 monograph, 5 scientific articles and
presented in 5 international conferences.
Te results of researches are used for academic courses and for supervising of
bachelor's and master's thesis in faculty of Geography and Earth Sciences of
University of Latvia.
Monograph
Gemste I., Smilga H., Ventiņš J. 2009. Notekūdeņu dūņas un augsne. Jelgava; LLU
Ūdenssaimniecības un zemes zinātniskais institūts, 272 lpp.
Scientific publications
Ventiņš, J. 1991. Latvijas meža augšņu lumbricīdu fauna. Jaunākais Mežsaimniecībā.
33. 105-109
Laiviņš M., Heniņa E., Kraukle M., Ventiņš J. 1993. The impact of the Saulkalne
lime processing facilities on the biotic diversity of pine forest. Proceedings of the
Latvian Academy of Sciences. B., 7: 552, 63-69
Ventiņš J. 1994. Earthworms (Lumbricidae) and some other groups of soil
mesofauna as bioindicators of eutrophication of dune soils in Jurmala. In: Proc. of
Int. Conf. "Coastal Conservation and Managemrnt in the Baltic Region", Klaipeda.
Vucāns A., Gemste I., Līvmanis J., Ventiņš J., Ivbulis P. 2000. Slieku izplatība
lauksaimniecībā izmantojamo platību augsnēs. LLU Raksti, 6, 22-29
Ventiņš J. 2011. Formation of earthworm (Oligochaeta, Lumbricidae) communities in
the most common soil types under intensive agricultural practice in Latvia. Proceedings
of the Latvian Academy of Sciences. B. (Pieņemts publicēšanai).
Abstracts of reports presented at international conferences
Ventiņš J. 1995. Earthworms (Lumbricidae) as bioindicators of eutrophication of
oligotrophic pine forest soils in Latvia. In: Proc. of 8th International Bioindicators
Symposium, Ceske Budejovice.
Ventiņš J., Gemste I., Vucāns A. 1999. Population dynamic of the earthworms
(Lumbricidae) in different agricultural soils in Latvia. In: Proc. Of International
conference "Biodiversity of Terrestrial and Soil invertebrates in the North",
Syktyvkar, Russia.
7

Ventins J. 2009. The main factors affecting earthworm (Lumbricidae) community in
most common types of agricultural soils in Latvia. In: Proc. of 12 th Nordic Soil
Zoology Symposium and PhD Course. Tartu, Estonia, August 28-31, 2009, pp. 111-
113.
Ventins J. 2010. Earthworm population dynamics under the impact of agricultural
practices and meteorological factors in the most common soil types in Latvia. The 9 th
International Symposium on Earthworm Ecology 5 th to 10 th September 2010, Xalapa,
Mexico. Book of Abstracts, p. 118
8

1. EARTHWORMS IN AGRICULTURAL LANDS
In Latvia has been found 8 earthworm genera with 13 species and one subspecies
(Ventiņš et al., 2009):
Allolobophora Eisen 1974 (sensu Perel, 1976)
A.chlorotica chlorotica (Savigny, 1826)
Aporrectodea Orley (sensu Perel, 1976)
A.caliginosa caliginosa (Savigny, 1826)
A.longa longa (Ude, 1885)
A.rosea rosea (Savigny, 1826)
A.limicola (Michaelsen, 1890)
Dendrobaena Eisen, 1874
D.octaedra Eisen, 1974
Dendrodrillus Omodeo, 1956 (sensu Perel, 1976)
D.rubidus subrubicundus (Eisen, 1874)
D.rubidus tenuis (Eisen, 1874)
Eisenia Malm, 1877 (sensu Perel, 1974)
E.foetida (Savigny, 1826)
Eiseniella Michaelsen, 1900
E.tetraedra tetraedra (Savigny, 1826)
Lumbricus Linnaeus, 1758
L.terrestris Linnaeus, 1978
L.castaneus (Savigny, 1826)
L.rubellus rubellus Hoffmeister, 1843
Octolasion Orley, 1885
O.lacteum (Orley, 1885)
The first regular researches of earthworm fauna in Latvia were initiated by V.
Eglitis (Эглитис, 1954) in 1946. In agricultural lands were found 10 earthworm
species, the most routinely found was Aporrectodea caliginosa. This species have
been found as far as 50 cm deep in the soils with acidicity pH 3.6- 7.8. It is one of the
9

most important species in the soil formation processes. Often found in agricultural
communities is also Lumbricus rubellus. Very important are also Aporrectodea rosea
and Lumbricus terrestris. Whereas in more acidic soils (pH 4.4- 5.3), e.g. peat, under
the moss on dolomite and sand, is found Dendrobaena octaedra. The richest
agriculture lands in earthworms are the loamy sod carbonate soils. In fields
earthworms normally live in the top 10 cm of the soil. In autumns they burrow
deeper in the soil. The earthworm population increases in perennial pasturelands,
whereas tillage has an adverse impact. The sandy soils shall be regularly cultivated
and fertilized, otherwise the population of earthworms reduces, or they may
disappear completely (Эглитис, 1954).
Earthworm dependence on soil properties have been widely researched in
Lithuania. According to data of O. Atlavinite (Атлавините, 1975), earthworms
mostly habit in loam, less in sandy loam, least in sandy soils and peatlands. The
dominant are such species as Aporrectodea caliginosa, Aporrectodea rosea and
Allolobophora chlorotica. The dominant species in the acidic podsol soils usually is
Dendrobaena octaedra. Often found are also Dendrodrillus rubidus tenuis and
Lumbricus rubellus. However, majority of earthworms prefer less acid, neutral soils,
reaching their maximum density at pH 6- 8. Distribution of the species is largerly
determined by the mechanical composition of the soil, content of the organic matter
and different agrotechnical activities (Атлавините, 1975; 1990).
In the most common agricultural soil types of Estonia are found 6 earthworm
species. The dominant is endogeic Aporrectodea caliginosa. Probably this species in
Estonia has occured only with development of agriculture. The second most usualy
found species is Lumbricus rubellus (Timm, 1970). Earthworm species Aporrectodea
caliginosa, Aporrectodea rosea and Lumbricus rubellus are characteristic to
intensively cultivated agricultural lands. Allolobophora chlorotica, Lumbricus
castaneus and anecic species are more sensitive to land cultivation. Their presence in
earthworm communities indicates on favorable agricultural conditions. The brown
soils are mentioned as the most appropriate for earthworms (Ivask et al., 2006; Ivask
et al., 2007).
10

Summing up data of numerous researches on the dominant earthworm species
in agricultural lands in Scandinavia, Central Europe and Eastern Europe, it has to be
concluded that the most common species is Aporrectodea caliginosa. Whereas in
acidic soils increases proportion of Dendrobaena octaedra and Lumbricus rubellus.
1.1. Earthworm impact on soil properties and microorganisms
Even in insignificant density earthworms may have great impact on soil aeration and
water infiltration. Earthworm presence may reduce soil compaction which has
occured due to agrotechnical activities. Earthworms have great impact on soil horizon
mixing, and dragging of the the upper layer, which is rich in organic matter, into the
deepest horizons (Lee, 1985; Curry, 1988).
Earthworms may have a significant impact on the chemical properties of the
soil. They drag down into the soil plenty of partly dispersed plant remains. In the
digestive tracts the remains are being macerated, mixed up with mineral particles of
the soil, enriched with Ca 2+ ions from calcium glands and returned to the soil as casts
(Stewart et al., 1980). Casts presence in the soil significantly improves its fertility.
The casts have a positive impact on aeration, water infiltration, quantity of water.
Increases soil active surface area, development of pore and channel system, which
allows the roots of plants to penetrate into the soil. In casts is being observed bacteria
and soil microscopic fungus activity increase. As well as the activity of
microorganisms is being stimulated in earthworm digestive tracts (Lee, 1985;
Schrader, Seibel, 2001). Increased activity of microbiological and digestive enzymes
is being observed in the central intestine of earthworms (Curry, Schmidt, 2007).
Researches indicate not only on symbiotic relations of earthworms and
microogranisms, but also on active use of microorgranisms as nutrition- especially
the species Aporrectodea caliginosa, which feeds on well decomposed detritus with
high concentration of microorganisms (Kristufek et al., 1994; Kristufek et al., 1995).
Other products of earthworm metabolism also descend into the soil (Lee, 1985).
Earthworms induce total oxygen mineralization in agricultural ecosystems. The
earthworm feeding activity increases content of oxygen available to plants in the soil,
11

especially increases content of nitrates (Bezkorovainaya et al., 2001). By increase of
earthworm density, increases also concentration of phosphorus forms for plants
(Атлавините, 1975, 1990; Lee, 1985).
1.2. Earthworms and soil cultivation
Conventional soil cultivation methods, such as tillage, disking, harrowing have
negative impact on the earthworm population. Tillage changes water content,
temperature, and aeration of the soil. Greater soil organism density is in agriculture
systems, where tillage is not used, because the soil structure and water stability are
maintained (Kladivko-Eileen, 2001; Miura et al., 2008). To Aporrectodea caliginosa
reasonable cultivation usually is favourable (Edwards, Lofty, 1973).
Influence of pesticides on the earthworm populations is ambiguous.
Fungicides, chlorous and phosphoric organic compounds usually have negative
impact, but after herbicide applications, earthworm population increase is being
observed, because expands their nutrition base - remains of weeds decaying tissue.
Lumbricus terrestris are very sensitive if herbicides are being applied to the soil
surface, whereas Aporrectodea caliginosa are more sensitive if herbicides are being
cultivated into the soil (Lee, 1985; Атлавините, 1990; Werner, 1990; Riley et al.,
2008).
Fertilizer influence on earthworms may be different. It is known that applying
of organic fertilizer usually has a positive impact on the earthworm populations.
Regarding the non-organic fertilizer use in agriculture and forestry, their impact is
ambiguous, and research results often are contradictionary.
One of the factors, having impact on the earthworm density in agricultural
lands, is plant culture. The perrenial cultures are more favorable to earthworms than
the one-year cultures. Activities of earthworms also have positive impact on plant
growth and harvest (Атлавините, 1990).
12

1.3. Earthworm impact on gricultural land quality bioindication
Earthworms are one of the most suitable soil organisms in the non-specific
bioindication. It is easy to identify them by few external morphological
characteristics. They are comparatively immobile, with stable sezonal taxocenosis
that eases population change determination. Also, it is much easier to get repetitions
of necessary samples, in order to obtain statistic representative data (Bauchhenβ,
2006).
Earthworms have impact on one of the most important processes of the soil-
organic matter breakdown and nutrition circulation. Earthworm fauna and its changes
actually reflect structural, microclimatic and nutrition circumstances of the soil, as
well as the toxicity of the soil (Kuhle, 1983). Change earthworm population,
biomass, ecological groups, structure and domination of the species. All of these
indicators reflect the antropogenic factors, e.g., after-effects of soil cultivation
(Christensen et al., 1987; Daugbjerg et al., 1988; Bauchhenβ, 2006). Stable
environment ensures constant species complexes during greater period of time, but in
non-stable environment, e.g., arable lands, species complexes are inconsistent and
lean (Lee, 1985). The structure of earthworm species communities is a good indicator
to assess the agroitechnical activity impact on soil. If more sensitive species are
found in agricultural lands, it indicates either on ecological factors suitable for
earthworms, or careful agrotechnical activities (Ivask et al., 2006; Ivask et al., 2007).
13

2. THE MONITORING SYSTEM OF AGRICULTURAL
LANDS
The State Agricultural Monitoring programme was initiated in 1992. It was based on
static observations of antropogenic load impact on agricultural lands in particular
obesrvation areas. With decree of Latvia State Land Service on February 14, 1994,
was affirmed „Regulation on monitoring of agricultural lands of the Republic of
Latvia” (Vucāns et al., 1996; 2000). In seven soil subspecies of three observation
areas, in the period from 1992 to 1998 was studied soil macrofauna, among them also
earthworms.
2.1. Descriptiom of the monitoring sampling plots
Earthworms were sampled in the following sampling plots of complex research areas-
Baldone parish, Riga region (Baldone 1- with higher relief location, Baldone 2- with
lower relief location) in sandy soil; Baldone K in drained marsh peat soil; Dobele
parish, Dobele region (Dobele 1- higher location, Dobele 2- lower) loamy soil;
Priekuli parish, Cesis region (Priekuli 1- higher location, Priekuli 2- lower) sandy
loam soil. Sampling plots were located in fields, which were used according to the
agricultural managemenet plans. Both sampling plots of Baldone were used as
perennial pasturelands. Dobele and Priekuli sampling plots during the observation
period were intensively cultivated- two times per season tilled, monocultures were
cultivated, pesticides and mineral fertilizers were applied. In each observation area, in
order to comprise the soil combinations located on different relief elements, two static
sampling plots of 10 x 10 m were established, one of a higher relief location, the
other- of a lower (in Baldone sampling plot of higher location the earthworm
population had not been formed, therefore it was excluded from data analysis). One
border of the sampling plot conformed to border of catena. In each plot randomly soil
samples were sampled with help of metal soil drill with diameter of 9.6 cm (drill
outlet area: 72.35 cm 2 ) up to 25cm depth. 30 samples were sampled once a year- at
the end of September, at the beginning of October- in the earthworm autumn activity
14

period. The samples were hand sorted. The found earthworms were fixed and kept in
formalin. Data on soil characteristics are summarized in Table 2.1.
Table 2.1
Chemical characteristics and granulometry of soils upper layer (0-20 cm) in
sample plots
Sample sites pH KCl
Baldone
(pasture)
Baldone K
(pasture)
Dobele 1 (intensively
cultivated)
Dobele 2 (intensively
cultivated)
Priekuļi 1 (intensively
cultivated)
Priekuļi 2 (intensively
cultivated)
Organic
matter %
Physical
clay %
Granulometry
of soils
5,5 3,2 9 Sandy
5,2 89 - Peat
7,2 1,4 29 Loamy
7,2 2,4 23 Loamy
5,4 1,8 19 Sandy loam
4,5 1,9 19 Sandy loam
2.2. Factors effecting earthworm density and community structure in the
monitoring sampling plots
The data obtained in agricultural land monitoring observation areas
demonstrate, that the most appropriate habitual environment for earthworms in
Latvia is in loamy soils. In particular areas of Dobele sampling plots, density of
earthworms extended even 300 worms m -2 . In the sandy loam soils of Priekuli, it is
considerably less. Relatively high density is also in the sandy soils of Baldone, but it
is considerably less in the peat soils (Figure 2.1, Table 2.2).
15

Table 2.2
Mean density (ind. m -2 ) and relative numbers (%) of earthworm species in sample plots
during observation period (1992 – 1998)
Dobele 1
Species 1992 1993 1994 1995 1996 1997 1998 % Total
Aporrectodea
caliginosa
68 136 323 277 49 182 80 96
Aporrectodea
rosea
5 2 0 0 0 0 0

Figure 2.1. All season mean density of earthworms per sample in sample plots. Columns
having equal letters are not statistically different (ANOVA, F-test; α = 0,05)
Field relief also has impact on earthworm populations. At the higher terrain
position, where soil surface erosion is more apparent, earthworm density may be
significantly less than in the lower part (Атлавините, 1975). Considerable factor,
which may have great impact in the dry summer months, is level of groundwater,
which in the lower parts of relief often is found closer to the soil surface. Comparing
earthworm density in the sampling plots of different relief location, it is evident that
the density is higher in the plots of lower relief location (Table 2.2). Especially it is
evident in Priekuli sampling plots. Differences in Dobele are less abvious.
Earthworm density dynamics in the sampling plots was greatly related with
meteorological conditions, especially with rainfall during the earthworm activity
period. After prolonged periods of dry and hot weather in summer (1992 and 1996),
the population of earthworms as a rule significantly reduced, whereas the increase of
the population was related with favorable humidity conditions in spring and summer
(1992, 1995 and 1997-1998). In Baldone sandy soils, which were not cultivated for a
longer period of time, the meteorological factors did not have such an impact.
Permanent vegetation (gramineae) on the surface of the soil forms such a protecting
layer, which reduces the impact of unfavorable meteorological conditions, thus
facilitating more even earthworm allocation in the soil.
Soil cultivation has a great impact on earthworm communities. In intensively
17

cultivated soils, earthworm density has significant seasonal fluctuations. Excessive
usage of pesticides and mineral fertilizers, and monoculture cultivation may be a
reason of the most sensitive species extinction. Aporrectodea caliginosa better than
any other species have adapted to soil cultivation (Lewis, 1980; Lee, 1985;
Атлавините, 1990), therefore, in the sampling plots (excluding the peat soil in
Baldone K) it is the dominant species (Table 2.2). Routinely in the sampling plots are
also found Lumbricus rubellus. The most intensive soile cultivation during the
observation period was in Priekuli sampling plots, what apparently is reason of
uncharacteristically low eathworm density for the sandy loam soils.
In the peat soil of Baldone K the dominat is Lumbricus rubellus. Frequent are
also acidophile Dendrobaena octaedra (Table 2.2). Aporrectodea caliginosa also
may form stable populations in peat soils however they spread later, characterizing
particular peat decomposition stage (Pižl, 1992).
Earthworm density and composition of species is a suitable indicator to assess
„health” or fertility of the agricultural soils. The omptimum earthworm density in
sandy loam and loam soils in Latvia should be more than 200 worm m -2 , but in sandy
soils- not less than 100 - 150 worms m -2 . In Baldone, in the perennial pastureland
soil, the density of earthworms during almost all the observation period is higher
than 130, or even 200 worm m -2 (Table 2.2). Whereas in Priekuli sampling plots the
density of earthworms is low during almost all the observation period, indicating on
unfavorable impact of agrotechnical activities on the earthworm populations. The
total earthworm density in Dobele sampling plots in favorable years is relatively
high. Zemgale loamy soils is one of the most suitable habitat for earthworms, and
with favorable meteorological conditions, even of intensive soil cultivation applied,
density of earthworms may significantly increase. However, the irregular fluctuaction
of the earthworm population during the years and significant dominance of
Aporrectodea caliginosa, indicate on instability of the population due to intensive
soil cultivation. In healthy soils usually are formed richer earthworm communities
with at least 3-5 species without particular one species dominance.
18

3. CHANGES OF EARTHWORM COMMUNITIES IN ACIDIC PINE
FOREST SOILS
3.1. Latvia’s oligotrophic forest soil earthworm fauna in Latvia and Northern
Europe
Latvia’s oligotrophic forest soil earthworm fauna has been little researched.
Comprehensive researches in the middle of the last centurie were carried out by
V.Eglitis (Эглитис, 1954). Lumbricus rubellus is mentioned as the dominant species.
Routinely found is also Lumbricus castaneus. Aporrectodea caliginosa is infrequent
in forests. The only earthworm species found in the dry pine forest stands is
Dendrobaena octaedra in density up to 10 worm m -2 , which inhabits the upper layer
of the soil just below the moss (Эглитис, 1954).
In the 70’s of the last century, in the Littoral lowland of Kurzeme, famous
Lithuanian lumbricologist O. Atlavinite (Атлавините, 1976) in a number of forest
types identified earthworm species structure and density. It was clarified that in the
dry pine forest with the typical podsol soils the dominant is Dendrobaena octaedra
up to 4 worm m -2 . Infrequent are Aporrectodea caliginosa and Lumbricus rubellus.
In the spruce forest podsol soils earthworm density is up to 40 worm m -2 (average 7.2
worms m -2 ). The dominant are Aporrectodea caliginosa and Lumbricus rubellus.
From 1977 to 1979, M.Šternbergs (Штернбергс, 1985), assessing Brocenu
cement and slate plant dust emission effect on the soil used earthworms as the
indicator organisms. In order to gather material numerous sampling plots were
created in the mast birch forest loam podsol soils. Species Aporrectodea rosea was
treated as a negative bioindicator of the forest soil pollution with dust from the
cement factory.
From 1988 to 1989 in Bulduri were carried out reaseraches on soil mulching
effect on the treaded Jurmala forest soil fauna (forest type Vaccinio myrtilli Pinetum).
In the monitoring sampling plot (podsol, pHKCl 3.75) was found uncharacteristic
earthworm density for the mentioned forest type- 51 worms m -2 with the dominant
species Lumbricus rubellus and Dendrobaena octaedra. In the sampling plot of the
treaded forest soil earthworms usually were not found, but in the mulched soil 4
19

earthworm species were found in density up to 164 worm m -2 (Ventiņš, 1991).
In Luthuania’s pine forests were found 4 earthworm species. The dominant is
Dendrobaena octaedra up to 3 worm m -2 . Is mentioned negative effect of conifers on
earthworms (Атлавините, 1976). T. Timm (Timm, 1970; 1999) indicates on
Dendrobaena octaedra and Lumbricus rubellus as the domimant species in Estonian
coniferous forests. Routinely found is also Dendrobaena octaedra and Lumbricus
rubellus, but in deciduous forests- Dendrobaena octaedra and Lumbricus rubellus.
In the coniferious forest of North-West Russia the dominant are such species as
Dendrobaena octaedra and Lumbricus rubellus in density up to 1 - 7 worms m -2 . It is
possible that earthworms in the Western lowlands of Russia spread from the Eastern
coast regions of the Baltic Sea. Freeze resistance, parthenogenesis, acido-tolerance,
ability to feed on low quality food, made such species as Dendrobaena octaedra
suitable to colonize the acid soils. With earthworms spreading into the forest soils,
organic and mineral soil horizons were gradually mixed (Tiunov, et al., 2006). With
change of the climate in the postglacial period and spread of deciduous tree species,
podsol began to change to the brown soils. That enabled also introduction of other
earthworm species (Räty, Huhta, 2004).
The big endogeic earthworms, e.g., Aporrectodea caliginosa, have greater
impact on soil processes than the epigeic species however their spread in the boreal
pine forests is restricted by soil acidity and freeze. In Finland’s pine forests (type
Vaccinum) dominance of Dendrobaena octaedra is almost of 85%. That is a species
with the widest habitat spectrum, however, in greater density it usually is found in
richer forest types, soils treated with lime, or in forests with great admixture of
deciduous trees. However, in the pine forests, earthworm density is not greater than 4
– 36 worms m -2 (Haimi, Einbork, 1992). In Sweden’s and Norway’s pine forest soils
(soil pH 3.5 – 4.5), the dominant are Dendrobaena octaedra, Dendrodrillus rubidus
tenuis, seldom Lumbricus rubellus 1,4 - 20 worms m -2 . Other species are rarely
found (Abrahamsen, 1972; Persson, 1988). According to the observations of the
author of the doctoral paper (unpublished data), in Sweden’s central part pine forest
areas alongside with Dendrobaena octaedra usually is found also Dendrodrillus
20

ubidus tenuis, whose propotion is increasing in the forest areas terated with lime.
3.2. Earthworm fauna changes due to forest liming
Although the boreal pine forest eutrophication and trasnformation processes
may be observed close to every bigger city of Northern and Central Europe, as well
as in territories where dynamic optional acctivities are being applied, therefore the
literature lacks of data on what effect do such changes have on the soil animals, and,
what is the possible soil animal impact on these processes. In Western Europe the
pine forest transformation problems are being considered by another point of view,
that is, in relation with forest liming, which is being implemented in order to improve
tree growth in poor soils and to reduce soil acidity caused by pollution (Robinson et
al., 1992a).
Several essential factors for earthworms are being changed by lime applicationsoil
acidity, content of calcium changes appear in microorganism consistence, which
are the potential nutritients, and others. After lime application, the earthworm density
as a rule increases. In Finland, after forest treatment with lime, esentially increased
population of Lumbricus rubellus, while population of Dendrobaena octaedra did
not change. It was observed that presence of Aporrectodea caliginosa reduces
population of Dendrobaena octaedra (Persson, 1988; Robinson et al., 1992).
Usually the most important reason of live animal population density increase is
the improvement of the nutritient base, or changes in the mutual competition of live
organisms (Persson, 1988). After lime application, reduces proportion of C:N in the
organic horizon of the soil (Zelles et al., 1990). Proportion C:N is one of the most
important earthworm population limiting factors (Lee, 1985). Conifers, moss and
lichen contain considerably less N and mineral substances than decidious trees and
vascular plants (Аристовская, 1980). Presence of vascular plant remains in O
horizon’s considerably favours increase of earthwomn population (McLean et al.,
1996). If soil acidity reduces, nitrogen mineralization happens faster, and increases
contrentation of the available nitrogen forms in the soil (Robinson et al., 1992a).
Earthworms facilitate different processes in the soil, including also formation of
21

primary production and nitrogen uptake (Huhta et al., 1998). In the areas where lime
has been applied, nitrogen mineralization happens even 50 times faster than in the
areas where lime has not been applied. These processes are more active after
introduction of the earthworm species Aporrectodea caliginosa (Robinson et al.,
1992b). Earthworms have positive impact on microorganisms of the forest soils.
They favor mycorriza formation and facilitate plant growth (Haimi, Einbork, 1992).
By increase of earthworm density and introduction of new species due to lime
application, increases also earthworm impact on the soil processes. Earthworms are
an essential factor in humus formation processes. Consequently changes the podsol,
and mull humus begins to form (Lee, 1985; Deleporte, Tillier, 1999). Dendrobaena
octaedra brakes down borders between the organic layers of the soil, mixing the
upper horizons of organic matter. Aporrectodea sp., Lumbricus rubellus, L.terrestris
intensively mixes the upper ground cover layers with mineral layers in depth of 25 to
30 cm, what to a certain extent may be compared to a tillage. In the boreal forest
areas of the USA, introducing in the forest soils different earthworm species at the
same time, in the organic horizon of the soil was observed soil raw humus (mor)
transformation into a mull structure with a well formed Ah horizon rich in organic
matter (Frelich et al., 2006).
3.3. Latvia’s boreal pine forest eutrophication and transformation
During the last decades intensive changes have been observed in Latvia’s pine
forest vegetation due to atmospheric deposition, climate changes, and land utilization
changes. Pine forest plant societies become less stable, numerous uncharacteristic
foreign species aggressively spread among them. Due to intensive spread of
gramineae species in the forests, enhances formation of sod. Organic matters
agglomerate in the upper layer of the soil, thus obstructing regeneration of conifer
trees (Laiviņš, Laiviņa, 1991; Laiviņš, 1998). Great impact is also of transboundary
transfer of the pollution (including nitrogene compounds) and emission from the
local pollution sources. Intensive use of dolomite and limestone in construction and
22

soil liming has facilitated great bulk of calcium and mangesium descending into the
forest soils. Due to what reduces acidity in the upper layer of the soil, changes the
upper layer structure and humus matter, and increases biomass of live organisms
(Мелецис, 1985; Laiviņš et al., 1993).
Most of the pine forests in Latvia are oligotrophic and mezotrophic dry forests.
In such forest types, mostly in suburbs and in towns, forest transformation processes
are more evident. Natural pine regeneration in such transformed forests is negligible.
Forest transformation is directly related to gradual eutrophication of the soils, due to
which increases the nutritient amount necessary to plants; and is related to reduction
of acidity, which significantly facilitates introduction of new species. The boreal
forests (Vaccinio vitis idaea-Pinetum, Vaccinio myrtilli-Pinetum) transform into
societies of much wider ground cover and underbrush content (Sambuco recemosae-
Pinetum). Forests become more shady and humid. The typical raw humus changes,
forming a transition form (moder humus) between mor and mull humus (Laiviņš,
Laiviņa, 1991; Laiviņš, 1998).
3.4. Earthworm species communities changes due to transformation of Jurmala
forest soils
3.4.1. Description of the sampling plots and sampling procedure
For the sampling plots was chosen Vaccinio myrtilli – Pinetum forest growth
type. In little transformed pine stands underbush and moss layer is well outlined,
whereas the transformed stands are easy to recongise for the uncharacteristic species
content and structure- dense bush, broad-leaved tree sprouts and vascular plants. It
allows both to assess the transformation level of the pine forests and to display main
stages of antropogenic succession (Laiviņš, 1998).
Earthworm material was sampled in September 1989 and May 1990 and
September of the same year, in the sampling plots of different eutrophication stages.
Sampling areas were chosen of similar relief location, humidity conditions, forest
stand age (middle age and adult stands) and soil composition. Soil type- typical
podsol on sand.
23

Two monitoring sampling plots were established in not transformed forests,
conformable to the basic association- in Pumpuri and Jaundubulti. Two sampling
plots established in Vaivari and Bulduri- in forests with signs of partial
eutrophication. Two sampling plots represent eutrophicated pine forests in Bulduri
and Dzintari, which were established in the antrophogenic association Sambuco
racemosae – Pinetum. Characteristic feature of the association is moss and bush
change to gramineae, as well as a dense bush storey (dominant species Sambuco
racemosa) and young deciduous trees. In the O horizon of the soil begins
degradation of the row mor humus and formation of the mull humus (Table 3.1)
(Laiviņš, Laiviņa, 1991)
Soil samples were gathered in the maximum earthworm activity period, in
spring and autumn, in each sample plot digging five 50 x 50 cm (0.25 m 2 ) soil holes
each up to 30 cm deep. The found earthworms were fixed and until identification
kept in 70% ethyl acohol.
Table 3.1
The thickness of soil upper horizons and chemical properties of soils in Jūrmala
sampleplots
* in Bulduri 2 and Dzintari are isolated transitional horizon AhE
Sample sites
Pumpuri
Jaundubulti
Vaivari
Bulduri 1
Bulduri 2*
Dzintari*
Soil
horizons
Thickness
of soil
horizons
cm
pHKCl
Organic
matter %
C:N
O1 3 3,5 93,6 -
O2 5 2,8 98,8 -
O1 6 3,8 90,1 36,4
O2 5 3,2 69,1 41,2
O1 1 4,4 79,9 28,2
OAh 9 4,1 66,3 29,6
O1 3 3,9 86,1 34,5
O2 (O Ah) 6 3,3 56,8 33,4
O1 1 - 67,9 29,1
O2 (O Ah) 5 5,2 52,4 28,5
O1 1 - 31,6 30
O2 (O Ah) 5 4,8 8,6 17,1
24

3.4.2. The total earthworm population density in Jurmala sampling plots
In all sample plots uncharectically high earthworm density was observed
(Table 3.2). Most of the earthworms were found in greatly eutrophicated plots
(Figure 3.1), but density was high also in the control plots. As in both control
sampling plots phytocenotic changes were not observed, it should be considered that
the earthworm populations on soil changes respond faster than the vegetation.
Table 3.2
Mean density (ind. m -2 ) and relative numbers (%) of earthworm species in Jūrmala
sample plots during observation period
Parauglaukums Suga
Dendrobaena
1989.g.rud. 1990.g.pav. 1990.g.rud. % total
octaedra
12,4
1,6
25,6
60
Pumpuri Lumbricus
rubellus
22,8
-
3,2
40
Kopā
Dendrobaena
35,2 1,6 28,8 100
octaedra
17,6
8,8
20,0
59
Jaundubulti Lumbricus
rubellus
22,4
-
9,2
41
Kopā
Dendrobaena
40 8,8 29,2 100
octaedra
Lumbricus
19,2
5,6
16
50
Vaivari rubellus
Aporrectodea
9,2
9,6
21,6
49
calliginosa
-
-
0,8
1
Kopā
Dendrobaena
28,4 15,2 38,4 100
octaedra
Lumbricus
20,8
11,6
25,2
46
Bulduri 1 rubellus
Lumbricus
23,2
12
20,4
45
castaneus
-
4,8
6
9
Kopā
Dendrobaena
44 28,4 51,6 100
octaedra
Lumbricus
26,8
21,6
10
35
rubellus
25,2
29,2
34,8
53
Bulduri 2
Lumbricus
castaneus
Aporrectodea
-
1,6
-
< 1
calliginosa
9,2
2
7,6
11
D.rub.ten.
-
-
0,8
< 1
Kopā 61,2 54,4 53,2 100
Dendrobaena
octaedra
2,8
5,6
8,4
9
Lumbricus
rubellus
48
25,2
36
61
Dzintari
Lumbricus
castaneus
Aporrectodea
calliginosa
D.rub.ten.
7,2
16,8
0,8
7,2
-
-
17,6
3,2
-
18
11
< 1
Octolasion
lacteum
-
0,8
-
< 1
Kopā 75,6 38,8 65,2 100
25

In spring of 1990, in both of the control sampling plots the earthworm
population significantly reduced (Table 3.2). In other sampling plots such sharp
population reduction was not observed. Obviously, it is related to changes of the soil
structure in the eutrophicated sampling plots and formation of humus horizon under
the O horizon. Such soils become habitable for earthworms not only in the upper
layer, but also in deeper layers, what enables them to migrate deeper in case of
unfavourable meteorological conditions. Therefore, earthworm density in
eutrophicated biocenosis is less subordinate to sezonal fluctuations, than in noneutrophicated-
the soils conformable to natural biotypes.
16
12
8
4
0
C
C
CB
Pumpuri Jaundubulti Vaivari Bulduri 1 Bulduri 2 Dzintari
Figure 3.1. All season mean density of earthworms per sample in Jūrmala
Sample plots. Columns having equal letters are not statistically different (ANOVA, Ftest;
α = 0,05)
3.4.3. Soil property change impact on earthworm communities
Greater diferences in soil acidity of upper horizons (O, OAh) in comparision
with other plots were observed in the eutrophicated sampling plots of Bulduri 2 and
Dzintari (Table 3.1). In the non-eutrophicated and partly eutrophicated sampling
plots the soils are assessed as very acid, but in both eutrophicated sampling plots pH
value corresponds to moderately acid soils. Taking into consideration the great
B
A
A
26

population of earthworms in all of the sampling plots it has to be concluded that the
soil acidity is not a determining factor on density increase.
The soil eutrophication processes are realated to increase of nutritients in the
soil and respectively also to increase of soil organism activity. Evidence of these
processes is reduction of nutritients in the upper horizonts of the soil. As a result
reduces content of mor humus, and start to form horizons of transitional type humus
(Laiviņš, Laiviņa 1991). Due to the disposing of nutritients improve also plant
growth conditions. Such soils are a more suitable living environment also for
earthworms, as evident by the increase in density. Very appropriate food for
earthworms is aboveground part remains and necrotic root residues of vascular
plants, as well as leaves of broad-leaved trees. Unlike needles, vascular plant remains
are richer in proteins and carbohydrates, as well as of lower C:N proportion
(Стриганова, 1980). Also the increase of bush and vascular plant storey density in
the eutrophicated sampling plots improves earthworm food ratio, at the same time
creating better soil shading and reducing humidity loss.
3.4.4. Earthworm communities structure in Jurmala sampling plots
One of the dominant species in almost all sampling plots is Dendrobaena
octaedra (Tables 3.2 and 3.3). Although density of these earthworms was detected
higher than normally in the similar forest type, however among the sampling plots,
independently on the eutrophication stage, differences in density are not great. The
second dominant species is Lumbricus rubellus. Its density significantly increases, if
increases the stage of environment eutrophication. In the monitoring sampling plots,
Lumbricus rubellus was found only in autumns, in other sampling plots- in all
seasons. In the monitoring sampling plots appropriate for earthworm habitation is
just the upper, thin ground cover of the soil (Table 3.1), which, in order to avoid the
impact of unfavorable meteorological conditions, limits Lumbricus rubellus
migration deeper in the soil. By the increase of the sampling plot eutrophication
stage, and simultaneously also by the increase of soil layer depth of the earthworm
habitat, seasonal density changes are not that evident anymore. In the eutrophicated
27

sampling plots, density of Lumbricus rubellus is high in all seasons. Aporrectodea
caliginosa were found only in greatly eutrophicated sampling plots. They were found
almost in all seasons that indicate on formation of a constant Aporrectodea
caliginosa population. Lumbricus castaneus is a typical forest species, and is not
normally found in acidic pine forest soils with pH value less than 4 (Атлавините,
1976). In Jurmala Lumbricus castaneus were found almost in all seasons in the
eutrophicated sampling plots, it may be due to both the decrease of soil acidity and
the incres of nutrition source- leave and vascular plant waste in the ground cover.
Table 3.3
Communitie of earthworms in Jūrmala sample plots in forests with different
degrees of eutrophication
*(Атлавините, 1976; unpublished data of author on earthworm fauna of oligotrophic
maritime pine forests in Western Latvia)
Observation site Communities of earthworms
Natural pine forests * Dendrobaena octaedra
Not transformed forests in Jūrmala Dendrobaena octaedra – Lumbricus rubellus
Forests with partial eutrophication in
Dendrobaena octaedra – Lumbricus rubellus
Jūrmala
Lumbricus rubellus – Dendrobaena octaedra –
Aporrectodea caliginosa
Eutrophicated forests in Jūrmala
Lumbricus rubellus – Dendrobaena octaedra –
Lumbricus castaneus - Aporrectodea caliginosa
To the non-eutrophicated sampling plots of Jurmala characteristic are
communities of two earthworm species Dendrobaena octaedra and Lumbricus
rubellus with little dominance of Dendrobaena octaedra (Tables 3.2 and 3.3). It
should be considered that formation of a stable Lumbricus rubellus population
indicates on the beginning of the eutrophication processes in these sampling plots. In
the partly eutrophicated sampling plots, increases dominance of Lumbricus rubellus.
Dominance of both Dendrobaena octaedra and Lumbricus rubellus here is
analagous. In the greatly eutrophicated areas appears typical dominace of Lumbricus
rubellus, but reduces dominance of Dendrobaena octaedra. Increases also population
28

of Aporrectodea caliginosa, emerge new earthworm species noncharacteristic to the
pine forest soils. Here are formed 3 to 4 earthworm species communities, who are
characteristic both- to conifer, and deciduous tree forests. They are considered as a
transition type species communities characterizing forest eutrophication processes. In
the non-eutrophicated pine forest soils such species communities have not been
found.
3.5. Earthworm communities change due to the industrial pollution in the pine
forests near Saulkalne
Saulkalne dolomite processing plant yearly emits into the atmosphere more
than 700 t of pollutants. In the 80’s of the last century, the production units
functioned in full load, but in the turn of the 80’s and 90’s, the production capacity
was rapidly decreased. The most common pollutants in the exausted emissions of the
factory are the dust containing calcium and magnesium compounds. Till 1995, when
installation of inovative purification filters was initiated the company operated
without strict requirements on the environmental protection (Vaivara, 2006).
3.5.1. Description of the sampling plots and sampling procedure
In order to determine the effect of the pollution created by Saulkalne dolomite
processing plant, in 1989 near the industrial area of Saulkalne were initiated lasting
observations on the forest dynamic. In the dominant wind direction for 6.3 km was
established transect with 5 sampling plots at different distances from the dolomite
processing factory (Table 3.4).
The sampling plots were created in areas, which conform to Vaccinio myrtilli –
Pinetum forest growth type. The forest stand age in 1989 was assessed to be from 41
to 63 years. Earthworms were sampled in the period from 1989 to 1991. The soil of
the sampling plots is formed of fine-grained sand. Organic matter and humus
accumulation horizon number in the first two sampling plots, closest to the emission
source, is higher (O, Ah, AhE). In these sampling plots, mineralization of the organic
29

matters happens more intense than in the furthest sampling plots, where just the
horizon O of organic matter was found (Table 3.5) (Laiviņš et al., 1993, Vaivara,
2006).
Table 3.4
The distance of te sample plots from the source of pollution and the hight above sea level
(Laiviņš et al., 1993)
Observation site Distance, m Height above sea level, m
Dolomite processing
plant
0 27,2
Saulkalne 1 300 28
Saulkalne 2 370 28
Saulkalne 3 1270 25
Saulkalne 4 4370 20,2
Saulkalne 5 6270 16,5
In the two sampling plots closest to the processing plant, the bush storey is well
developed. The vegetation according to the Elenberg scale corresponds to a
moderately rich, neutral soil. Also the bush storey of Saulkalne 3 is well developed.
The vegetation corresponds to a moderately rich, moderately acidic up to a neutral
soil. Saulkalne 4 and 5 correspond to an acidic, poor soil. The furthest sampling plot
was chosen as a control plot, as according to the vegetation it corresponded to a
Vaccinio myrtilli – Pinetum forest type. Other sampling plots correspond to a same
forest type of different stages of degradation (or europhication) (Laiviņš et al., 1993;
Laiviņš, 1998; Vaivara, 2006).
Soil samples were taken in the period of maximum earthworm activity, in
spring and autumn, in each plot digging five 50 x 50 cm (0.25 m 2 ) soil holes up to
the upper border of horizon B. The found earthworms were fixed and till
identification kept in a 70% ethyl alcohol.
30

Table 3.5
The chemical properties of soil upper horizons in Saulkalne sample plots
(Laiviņš et al., 1993; Vaivara, 2006)
Sample
plots
1
2
3
Soil horizons pH KCl C:N Ca, ppm Mg, ppm
O1 7,1 15 56000 1800
Ah 6,2 10 38000 1700
O1 6,3 14 74000 1820
Ah 6,2 8 14000 1450
O1 6,5 14 500 90
Ah E 6,5 9 750 380
O1 5,4 19 750 280
4 O2 4,7 16 850 300
O1 4,7 19 1800 350
5 O2 4,4 14 980 320
3.5.2. The total earthworm population in Saulkalne sampling plots
In Saulkalne transect sampling plots were found 6 earthworm species, among
them two subspecies of one species (Table 3.6). As characteristic to the acidic forest
soils must be mentioned Dendrobaena octaedra and Dendrodrilus rubidus tenuis.
Earthworm density in all the sampling plots was relatively high. That refers not only
to the closest sampling plots to the factory, with well evident signs of eutrophication,
but also to the furthest two sampling plots, where eutrophication signs in the
vegetation are little evident or not evident at all. The highest density was found in
both closest sampling plots to the factories - Saulkalne 1 and Saulkalne 2. During the
obesrvation period the density in these sampling plots tended to increase. The
earthworm density in the sampling plot Saulkalne 3 also showed a relevant tendency
to increase. In the furthest two sampling plots such population increase was not
detected. In all the three furthest sampling plots relevant seasonal changes were
observed- the density was increasing in autumn, but decreasing in spring.
31

Table 3.6
Saulaklnes parauglaukumos ievāktās slieku sugas, to blīvums (ind. m -2 ) un relatīvais
skaits
* - distance from the source of pollution
Sample plots.
Distance *
Saulkalne 1
300 m
Saulaklne 2
370 m
Saulaklne 3
1270 m
Saulaklne 4
4370 m
Saulaklne 5
6270 m
Species
Dendrobaena
octaedra
Lumbricus
rubellus
Aporrectodea
caliginosa
D.rub.ten.
D.rub.subr.
Autumn of
1989
0,8
5,6
0,8
1,6
0
Spring of
1990
1,6
11,6
2,8
0
0
Autumn of
1990
12,8
20,4
12,4
0
0,8
Spring of
1991
8,8
6,4
6,0
0
0
% total
Kopā 8,8 16 46,4 21,2 100
Dendrobaena
octaedra
Lumbricus
rubellus
Aporrectodea
caliginosa
D.rub.ten.
0,8
8,0
2,8
0
1,6
11,6
9,6
0
Kopā 11,6 22,8 35,6 42,4 100
Dendrobaena
octaedra
Lumbricus
rubellus
Aporrectodea
caliginosa
Lumbricus
castaneus
Eisenia foetida
2,4
9,2
9,2
0,8
0,8
6,0
2,8
0
0
0,8
Kopā 22,4 9,6 36,8 33,2 100
Dendrobaena
octaedra
Lumbricus
rubellus
Aporrectodea
caliginosa
D.rub.ten.
10,4
12,0
0
0
11,2
1,6
0
1,6
Kopā 22,4 14,4 21,6 10 100
Dendrobaena
octaedra
Lumbricus
rubellus
D.rub.ten.
6,0
10,0
0
18,0
6,8
0,8
Kopā 16 25,6 19,2 12 100
12,4
17,6
5,6
0
4,8
12,8
18,4
0
0,8
5,6
13,6
0
2,4
6,4
12,8
0
18,4
13,6
9,6
0,8
2,4
11,2
18,8
0
0,8
0,8
5,2
1,6
2,4
1,6
9,6
0,8
26
48
24
< 2
< 1
30
45
25
< 1
15
35
46
1
3
41
47
2
10
44
54
2
32

For the reciprocal comparision of the sampling plots the average density of
worms in all seasons was chosen (Figure 3.2). In comparision with natural forests of
similar growth type, the average earthworm density in Saulkalne sampling plots is
relatively high. Even in the monitoring sampling plot with vegetation corresponding
to a natural forest type, the density in all seasons is heightened. Obsviously, also in
Saulkalne sampling plots, changes in the earthworm populations are observed before
changes in the vegetation.
8
6
4
2
0
Saulk 1 Saulk 2 Saulk 3 Saulk 4 Saulk 5
Figure 3.2. All season mean density of earthworms per sample in Saulkalne sample plots.
In highly transformed forests, closer to the emission source, the earthworm
population has a tendency to increase. In the closest sampling plot to the factory, the
density is little lower than in the next two, what may be due to the emited pollution
of factorie in they direct closiness. In the both furthest sampling plots, where the soil
pollution level is lower, the earthworm density is lower. However, ANOVA analysis
did not show significant differences among the sampling plots.
Comparing seasonal earthworm changes, it is evident, that in the sampling
plots Saulkalne 1 and Saulkalne 2, the density gradually increases. Such a
nonchaectaristic earthworm population dynamics to the pine forest biotypes
33

obviously is related to the already mentioned reduction of factory operational
activity.
3.5.3. Pollution impact on the earthworm populations
Changes in the earthworm population in the sampling plots are related to the
factory emited pollution impact on the pine forest biocenosis. As evident from the
obtained data, in Saulkalne 1 and Saulkalne 2 the relatively high concentration of
calcium and magnesium in the soil does not have a direct impact on the earthworm
populations. The other way round, Saulkalne 2, where the highest concentration of
these metals in the soil surface was found, the highest total average all season
earthworm density was observed. It should be concluded that the calcium and
mangesium compund impact on the soil acidicity is more critical to the earthworm
populations. In all the sampling plots of transect the found soil acidity is relatively
low (Table 3.5). In the closest sampling plots to the emission source, it is evaluated
as a fairly acid- neutral or even alkaline. Also in the two furthest sampling plots, pH
values in the soil surface are relatively high and correspond to acid or moderately
acid soils. Due to the soil acidicity reduction, increases activity of microorganisms,
improves plant growth conditions, lowers proportion of C:N (Zelles et al., 1990), as
well as reduces the deliquescence of aluminium compounds and improves Ca and
Mg consuming to the soil organisms (Аристовская, 1980; Cronan, Grigal, 1995). In
the closest sampling plots to the emission source, the C:N proportion is favorable to
earthworms and other organisms of the soil. In the both furthest sampling plots, its
values are under 20, that indicates on the mineralization processes activization.
3.5.4. The earthworm communities structure in Saulkalne sampling plots
Comparing the density of Dendrobaena octaedra, no considerable differences
are observed in the sampling plots. In the furthest sampling plots routinely was found
another species of acidic soils- Dendrodrillus rubidus tenuis. The increase of the
population of this species in the forest areas where lime has been applied was
34

observed by the author of the doctoral paper in 1993, in central Sweden’s pine forests
soils (unpublished data). T.Persson also (Persson, 1988) indicates on the increase of
Dendrodrillus rubidus tenuis population after the lime application to the pine forests
in Sweden and Germany. Possible, that Dendrodrillus rubidus tenuis is one of the
indicating species of the lime compound polluted pine forest soils. The density of
Lumbricus rubellus is relatively high in all sampling plots. Greater population of
Aporrectodea caliginosa was found in the sampling plot Saulkalne 3. Although in the
two closest sampling plots to the emission source they were found in a fewer number
(probably due to the impact of pollution). However, in all three sampling plots the
species has formed stable populations, what is realated to formation of humus Ah
horizon. In both furhest sampling plots, where formation of horizon Ah was not
observed, just few specimen of Aporrectodea caliginosa were found.
The dominant species in all sampling plots of Saulkalne transect is Lumbricus
rubellus. A communitie of two species- Lumbricus rubellus - Dendrobaena octaedra
is characteristic for the furthest two sampling plots. In three sampling plots closest to
the emission source, great number of Dendrobaena octaedra and Aporrectodea
caliginosa also was found, thus forming a communitie of three species (Table 3.7).
Sample plots
Slieku sugu cenozes Saulkalnes transekta parauglaukumos
Distance from the source of
pollution, m
Saulkalne 1 300
Saulkalne 2 370
Saulkalne 3 1270
Saulkalne 4 4370
Saulkalne 5 6270
Communities of earthworms
3.7. tabula
Lumbricus rubellus – Dendrobaena
octaedra – Aporrectodea caliginosa
Lumbricus rubellus – Dendrobaena
octaedra – Aporrectodea caliginosa
Lumbricus rubellus – Aporrectodea
caliginosa – Dendrobaena octaedra
Lumbricus rubellus – Dendrobaena
octaedra
Lumbricus rubellus – Dendrobaena
octaedra
35

3.6. The potential earthworm impact on processes of soil eutrophication in the
forests of Jurmala and Saulkalne
Increase of the total earthworm population has impact on both the soil structure
and its fertility (Lee, 1985; Атлавините, 1990; Haimi, Boucelham, 1991; Deleporte,
Tillier, 1999; McInerney et al., 2001; Räty, Huhta, 2004). The earthworm population
increase may be related to the possible microorganism activization in the non-
degradated sampling plots in Jurmala and Saulkalne after additional nutritient
spreading into the forest soils due to the recreative load, optional activities and
pollution (Figure 3.3). Activity of microorganisms quickens decomposition of plant
residues, and greater amount of nutritients descend into the soil, creating favorable
circumstances for the earthworm population increase, and plant growth. In the gullets
of earthworms occurs formation of humus matter with more neutral pH reaction,
forming stable aggregates with soil mineral complexes. It reduces the processes of
soil podsolation (Аристовская, 1980; Стриганова, 1980). Especially active forest
plant residues recyclers and soil formers are Lumbricus rubellus, whose population
increase and the dominance in species communities have been observed in both-
Jurmala, and Saulkalne. Significant is formation of a stable population of endogeic
Aporrectodea caliginosa. Presence of earthworms may become a significant factor
for the further biocenosis development. Earthworms quicken different processes in
the soil, among them also formation of primary production, mineralization and
accumulation of nitrogene, formation of mull humus (Satchell, 1980; Стриганова,
1980; Tiunov, Scheu, 2004). It means that in the forest transformation processes in
both- Jurmala, and Saulkalne, more significant are the inner factors of the
biocenosis- the mutual incentive impact of microorganisms, earthworms and plants.
36

Figure 3.3. Possible process of pine forests eutrophication and role of earthworms on
bioindication of different stages of eutrophication
3.7. Role of earthworms in the bioindication of the pine forest eutrophication
processes
Changes of earthworm fauna reflect the soil processes. Earthworm
communities are sensitive to the forest transformation processes, forming species
complexes appropriate for the soil and forest growth condition type. Also changes
earthworm density, ecological groups, species structure and dominance structure
((Bauchhenβ, 2006). Earthworms are an appropriate soil animal group in the nonspecific
bioindication of oligotrophic pine forest transformation (eutrophication).
Dynamics of the earthworm species and changes of the species structures, very
well reflect complex biocenotic changes due to both the increase of forest recreation
loads and the calcium pollution. As researches in Jurmala and Saulkalne transect
soils show, changes in earthworm communities are detected before the fitocenotic
37

changes. That allows to identify soil eutrophication already in its initial stages. The
most important quantitative indicators reflecting these processes are increase of the
total earthworm population, and formation of a stable Lumbricus rubellus population.
Further stages of eutrophication processes feature changes of the earthworm
communitie dominance structure- Dendrobaena octaedra, as the dominant species in
natural forests, is replaced by Lumbricus rubellus. Greatly eutrophicated biotypes are
characterized with formation of 3 to 4 species communities and diversification of the
earthworm ecological groups. Very essential is formation of the endogeic
populations, especially Aporrectodea caliginosa, what may occur only in a particular
stage of the organic matter decomposition (Стриганова, 1980). Aporrectodea
caliginosa is one of the most important soil animal representatives, which as a key
species may significantly influence and quicken both processes in the soil and
processes of the ecosystem. Formation of a stable population of Aporrectodea
caliginosa may indicate on irreversible changes in the soil. However, pine forest
eutrophication final stages may be easily identified by fitocenotic changes.
Earthworms, as a bioindicator of these processes, have greater significance in the
indication of the initial stages.
38

CONCLUSIONS
1. Reasearches conducted within the framework of Latvia’s agricultural land
monitoring, showed that the total earthworm population density and number of
species in Latvia are determined by the soil type and the granulometry of soil. The
highest earthworm density is characteristic for loamy soils, but the least- to sandy
soils which are poor in organic matter.
2. The earthworm population is influenced by the field relief. On the top of
hillocks, where the soil erosion is more evident, the earthworm density is less than in
the bottom layer, which is rich in humus.
3. The earthworm density dynamics is influenced by rainfall in the period of
earthworm acitivity. Land cultivation enhances the earthworm population sensitivity
to the meteorological factors. In agricultural lands, which have not been cultivated
for a while, the impact of the meteorological factors is not that evident, and the
earthworm population distribution in the soil is more even.
4. In intesively cultivated soils, the earthworm density and number of
species reduces. Aporrectodea caliginosa, in comparision with other species, has
adapted the best to the soil cultivation. Its dominance can reach even 100%.
5. The earthworm density and the species structure is an appropriate
indicator to detect „health” and fertility of the agricultural soils. The optimum
earthworm density in loamy soils and sandy loam soils in Latvia is not less than 200
worms m -2 , but in sandy soils not less than 100 - 150 worms m -2 . In fertile soils and
with favorable conditions, occurs formation of rich earthworm communities with 3 to
5 species, one or two of which are dominant. Reduction of the earthworm species
population indicates on the increase of soil degradation processes.
6. In researches on oligotrophic pine forest soil eutrophication due to the
recreation load in Jurmala and due to the industrial lime containing pollution near
Saulkalne dolomite processing plant, altogether were found 8 earthworm species and
one subspecies. In both Jurmala and Saulkalne analogous tendencies were
characteristic in the earthworm cenosies changes. The most important reason for it is
the improvement of earthworm nutrition conditions. Increases number of species,
39

changes dominance structure, Dendrobaena octaedra is replaced by Lumbricus
rubellus. Populations of endogeic Aporrectodea caliginosa form in greatly
eutrophicated biocommunities.
7. Formation of humus horizon in the eutrophicated soils create additional
living-space for earthworms, both with appropriate feeding conditions and possibility
to migrate into deeper layers in case of unfavorable meteorological conditions.
8. Earthwrom activities in the eutrophicated forest soils become an essential
inner factor of the biocenosis, and initiate further soil transformation process.
Earthworms improve physical soil properties, activate breakdown of the organic
matter and their spread into the soil profile, thus promoting formation of thicker
humus horizon. Close to the populated areas establishment of new earthworm
populations occur faster than in isolated forest areas, therefore, in such areas quicken
the forest eutrophication processes.
9. Earthworms are considered as great indicatiors of the oligotrophic pine
forest eutrophication processes. The most important bioindicative indicators in the
initial stages of the eutrophication processes are the total earthworm population
density increase, 3 to 4 species earthworm communities, formation of a stable
Lumbricus rubellus population, and expansion of the ecological group spectrum.
10. Changes in earthworm communities are being detected before visual
changes in the forest phytocenosis. That allows to identify soil eutrophication in its
initial stages.
40

LITERATURE
Abrahamsen, G. 1972. Ecological study of Lumbricidae (Oligochaeta) in Norwegian
coniferous forest soils. Pedobiologia, 12, 267-281.
Bauchhenβ, J. 2006. Regenwürmer als Bioindikatoren Bodenzoologische
Untersuchungen auf BDF. Bodenbiologische Bewertung von Bodendauerbeobachtungsflächen
(BDF) anhand von Lumbriciden. Workshop in Weimar,
22-32.
Bezkorovainaya, I., Klimentenok, L., Efvgrafova, S. 2001. Dynamics of the
biological activity of litter as it is transformed by earthworm. Biology Bulletin. 28
(2), 188–190.
Christensen, O., Daugbjerg, P., Hinge, J., Jensen, J.P., Sigurdardottir, H. 1987.
Effekten af dyrkningspraksis pa regnorme og deres mulige rolle som bioindikatorer.
Særtryk af Tidsskrift for Planteavl, 91, 15-32.
Coûteaux, M.M., Bolger, T. 2000. Interactions between atmospheric CO 2 enrichment
and soil fauna. Plant and Soil, 224, 123–134.
Cronan, C.S., Grigal, D.F. 1995. Use of calcium/aluminum ratios as indicators of
stress in forest ecosystems. Journal of Environmental Quality. 24, 209-226.
Curry, J. 1988. The ecology of earthworms in reclaimed soils and their influence on
soil fertility. In: Earthworms in Waste and Environmental Management. Clive, A.E.,
Neuhauser, E.F. (ed.). The Hague: SPB Academic Publishing, 251-261.
Curry, J.P., Schmidt, O. 2007. The feeding ecology of earthworms – A review.
Pedobilogia, 50, 463 – 477.
Darwin, C.R. 1881. The Formation of Vegetable Mould through the Action of Worms,
with Observations on Their Habits. Murray, London. 326 pp.
Daugbjerg, P., Hinge, J., Jensen, J., Sigurdardottir, H. 1988. Earthworms as
bioindicators of cultivated soils? Ecological Bulletins, 39, 45–47.
Deleporte, S., Tillier, P. 1999. Long-term effects of mineral amandments on soil
fauna and humus in an acid beech forest floor. Forest Ecology and Management, 118,
245-252.
Edwards, C., Lofty, J. 1975. The influence of cultivations on soil animal populations.
Progress in Soil Zoology. Proc. 5th International Coloquium on Soil Zoology,
Prague, 1973. Vanek, J. (ed.). pp. 399-407.
41

Frelich, L., Hale, C., Scheu, S., Holdsworth, A., Heneghan, L., Bohlen, P., Reich, P.
2006. Earthworm invasion into previously earthworm-free temperate and boreal
forests. Biol Invasions, 8, 1235-1245.
Gemste, I., Smilga, H., Ventiņš, J. 2009. Notekūdeņu dūņas un augsne. Jelgava, LLU,
272 lpp.
Lee, K. E. 1985. Earthworms. Their Ecology and Relationships with Soil and Land
Use. Sydney, Orland, London, Academic Press, pp. 411.
Haimi, J., Boucelham, M. 1991. Influence of a litter feeding earthworm, Lumbricus
rubellus, on soil processes in a simulated coniferous forest floor. Pedobiologia 38,
247-256.
Haimi, J., Einbork, M. 1992. Effects of endogeic earthworms on soil processes and
plant growth in coniferous forest soil. Biol.Fertil Soils,13, 6-10.
Huhta, V., Persson, T., Setälä. 1998. Functional implications of soil fauna diversity in
boreal forest. Applied Soil Ecology, 10, 277-288.
Ivask, M., Kuu, A., Sizov, E. 2007. Abundance of earthworm species in Estonian
arable soils. Eur. J. Soil Biol., 43, 39-42.
Ivask, M., Kuu, A., Truu, M., Truu, J. 2006. The effect of soil type and soil moisture
on earthworm communities. Agraarteadus, XVII (1), 3-33.
Kladivko-Eileen, J. 2001. Tillage systems and soil ecology. Soil and Tillage
Research, 61 (1-2), 61-76.
Kristufek, V., Pižl, V., Ravasz, K. 1995. Epifluorescent microscopy of earthworms
intestinal bacteria. Acta Microbiologica et Immunologica Hungarica, 42 (1), 39-44.
Kristufek, V., Tajovsky, K., Pižl, V. 1994. Ultrastructural analysis of the intestinal
content of earthworm Lumbricus rubellus Hoffm. (Annelida, Lumbricidae). Acta
Microbiologica et Immunologica Hungarica, 41 (3), 283-290.
Kuhle, J. 1983. Adaption of earthworm populations to different soil treatments in
apple orchard. In: Proc. VIII. Int. Colloq. Soil Zool., Louvain-la-Neuve, Belgium,
1982. Andre, H.M., De Medts, A., Gregoire-Wibo, C., Wauthy, G. (eds.), 487-501.
Laiviņš, M. 1998. Latvijas boreālo priežu mežu sinantropizācija un eitrofikācija.
Latvijas Veģetācija, 1, 137. lpp.
Laiviņš, M., Heniņa, E., Kraukle, M., Ventiņš, J. 1993. The impact of the Saulkalne
lime processing facilities on the biotic diversity of pine forest. Proceedings of the
42

Latvian Academy of Sciences, B, 7 (552), 63-69.
Laiviņš, M., Laiviņa, S. 1991. Jūrmalas mežu sinantropizācija. Jaunākais
Mežsaimniecībā, 33, 67-83.
Lewis, T. 1980. Faunal change and potential pests associated with direct drilling.
EPPO Bull., 10 (2): 187-193.
McInerney, M., Little, D., Bolger, T. 2001. Effect of earthworm cast formation on the
stabilization of organic matter in fine soil fractions. Eur. J. Soil Biol., 37, 251-254.
McLean, M.A., Kolodka, D.U., Parkinson, D. 1996. Survival and growth of
Dendrobaena octaedra (Savigny) in pine forest floor materials. Pedobiologia, 40,
281-288.
Miura, F., Nakamoto, T., Kaneda, S., Okano, S., Nakajima, M., Murakami, T. 2008.
Dynamic of soil biota at different depths under two contrasting tillage practices. Soil
Biology and Biochemistry, 40 (2), 406-414.
Paoletti, M. 1999. The role of earthworms for assessment of sustainability and as
bioindicators. Agriculture, Ecosystems and Environment, 74, 137-155.
Persson, T. 1988. Effects of liming on the soil fauna in forest – a literature review.
Statens naturvårdsverk, Rapport 3418, pp. 92.
Pižl, V. 1992. Succession of earthworm populations in abandoned fields. Soil Biol.
Biochem., 24 (12), 1623-1628.
Räty, M., Huhta, V. 2004. Earthworm communities in birch stands with different
origin in central Finland. Pedobiologia, 48 (3), 283-291.
Riley, H., Pommeresche, R., Eltun, R., Hansen, S., Korsaeth, A. 2008. Soil structure,
organic mater and earthworm activity in a comparison of cropping systems with
contrasting tillage, rotations, fertilizer levels and manure use. Agriculture,
Ecosystems & Environment, 124 (3-4), 275-284.
Robinson, C.H., Piearce, T.G., Ineson, P., Dickson, D.A., Nys, C. 1992a. Earthworm
communities of limed coniferous soils: field observations and implications for forest
management. Forest Ecology and Management, 55, 117-134.
Robinson, C.H., Ineson, P., Piearce, T.G., Rowland, A.P. 1992b. Nitrogen
mobilization by earthworms in limed peat soils under Picea sitchensis. Journal of
Applied Ecology, 29, 226-237.
Schrader, S., Seibel, C. 2001. Impact of cultivation management in agroecosystem.
43

Eur. J. Soil Biol., 37, 309-313
Stewart, V., Salih R., Al-Bakri, K., Strong, J. 1980. Earthworms and soil structure.
Welsh Soils Discussion Group Report, 21, 103-114.
Satchell, J.E. 1980. r worms and K worms: A Basis for classifying lumbricid
earthworms strategies. In: Soil Biology as Related to Land Use Practicies. Dindal,
D.L. (ed.) Proc. VII Internatinal Soil Zoology Colloquium, EPA, Washington, D.C.,
pp. 848 – 854.
Timm, T.A. 1970. On the fauna of the Estonian Oligochaeta. Pedobiologia, 10, 52-
78.
Timm, T. A. 1999. Guide ti the Estonian Annelida. Estonian Academy Publishers.
Tartu-Tallin, 208 pp.
Tiunov, A., Hale, C., Holdsworth, A., Vsevolodova-Perel, T. 2006. Invasion patterns
of Lumbricidae into the previously earthworm-free areas of northeastern Europe and
the westeren Great Lakes region of North America. Biol. Invasions, 8, 1223-1234.
Tiunov, A., Scheu, S. 2004. Carbon availability controls the growth of detritivores
(Lumbricidae) and their effect on nitrogen mineralization. Oecologia, 138, 83-90.
Vaivara, E. 2006. Priežu mežu struktūra un dinamika Saulkalnes rūpnīcu
piesārņojuma zonā. Maģistra darbs, Rīga, LU ĢZZF, 109. lpp.
Ventiņš, J. 1991. Latvijas meža augšņu lumbricīdu fauna. Jaunākais Mežsaimniecībā.
33.105-109
Ventiņš J., Vucāns A., Gemste I., Līvmanis J., Ivbulis P. 2000. Slieku izplatība
lauksaimniecībā izmantojamo platību augsnēs. LLU Raksti 6, 22-29
Vucāns, A., Gemste, I., Kārkliņš, A. 1996. Lauksaimniecībā izmantojamās zemes
pārraudzības komplekso novērojumu pirmo gadu (1992-1995) rezultāti. LLU Raksti,
6, 42-54.
Zelles, L., Stepper, K., Zsolnay, A. 1990. The effect of lime on microbial activity in
spruce (Picea abies L.) forest. Biol. Fertil. Soils, 9, 78-82.
Аристовская, Т.В.1980. Микробиология процессов почвообразования.
Ленинград. Наука, 187 с.
Атлавините, О. 1975. Экология дождевых червей и их влияние на плодородие
почвы в Литовской ССР. Вильнюс, Мокслас, 202 с.
Атлавините, О. 1976. Lumbricidae. В кн.: Фауна почвенных
44

беспозвоночныхморского побережя Прыбалтики. Вильнюс, Мокслас, 49-52 с
Атлавините, О. 1990. Влияние дождевых червей на агроценозы. Вильнюс,
Мокслас, 179 с.
Эглитис. В.1954. Фауна почв Латвийской ССР. АН ЛССР. 261 с.
Перель, Т.С. 1979. Распространение и закономерности распределение
дождевых червей в фауне CCCP. Москва, Наука, 272 с.
Стриганова. Б.Р. 1980. Питание почвенных сапрофагов. Москва, Наука, 243 с.
Штернбергс, М. 1985. Воздеиствие выбросов цементного завода на дождевых
червей (Lumbricidae) березняков-кисличников. В. Кн.: Загрязнение природной
среды кальцийсодержащей пылю. Рига, Зинатне, 96-100 с.
Мелецис. В. 1985. Биоиндикационное значение коллембол (Collembola) при
загрязнении почвы березняка-кисличника индустриальной кальцийсодержащей
пылю. В. Кн.: Загрязнение природной среды кальцийсодержащей пылю. Рига,
Зинатне,
Werner, M.R. 1990. Earthworm ecology and sustaining agriculture:
www.sarep.ucdavis.edu/worms/werner.htm, 23. jūlijs 2008.
45