Industrial Crops and Products 66 (2015) 206–209
Contents lists available at
Industrial Crops and Products
j o u r n a l h o m e p a g e :
w w w . e l s e v i e r . c o m / l o c a t e / i n d c r o p
Influence of biogas digestate on density, biomass and community
composition of earthworms
Barbara Koblenz
, Sabine Tischer
, Jan Rücknagel
, Olaf Christen
a
University of Halle-Wittenberg, Institute of Agricultural and Nutritional Sciences, Agronomy and Organic Farming, Betty-Heimann-Straße 5, 06120 Halle
(Saale), Germany
b
University of Halle-Wittenberg, Institute of Agricultural and Nutritional Sciences, Soil Biogeochemistry, Germany
a r t i c l e i n f o
Article history:
Received 10 September 2014
Received in revised form
20 November 2014
Accepted 13 December 2014
Available online 8 January 2015
Keywords:
Biogas digestate
Slurry
Earthworms
Community composition
Biogas plants
a b s t r a c t
In recent years, the increasing number of biogas plants in operation has also led to a considerable rise in
fermentative substrates, which are now widely used as agricultural fertilizers. The impact on earthworm
fauna of using biogas digestate as a fertilizer has yet to be sufficiently researched. At two different tests
sites, the short-term (four months after fertilization) and longer-term (three-year test period) influence
of using fermented residues as a fertilizer was examined on earthworm density, biomass and community
composition compared to using traditional fertilizers (cattle and pig slurry, chemical fertilizers as well
as an unfertilized control). The crop grown was maize (Zea mays L.). Applying biogas digestate and slurry
had a positive overall impact at both sites on earthworm density and biomass. Observing different fer-
tilization regimes in the short term, the significantly highest earthworm density was seen where slurry
had been applied. In the treatments with digestate and conventional slurry, earthworm biomass differed
significantly in comparison with chemical fertilization and the untreated variant. After three years, earth-
worm biomass in the variants fertilized with conventional slurry and digestate tended to be higher than
in the chemical fertilizer and untreated variants. Community composition was strongly influenced by the
application of digestate. A decrease in the species Aporrectodea rosea was accompanied by an increase in
Aporrectodea caliginosa. The earthworm population was supported equally positively at both sites by the
variants with conventional slurry and digestate.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
In recent years, the promotion of renewable energy generation
has resulted in a significant increase in the importance of agri-
cultural biogas production (
). In addition to biogas,
digestate is a by-product of microbial anaerobic digestion (
). The considerable amounts of digestate that accumu-
late are now being used more widely as secondary fertilizers in
agriculture. So far it has not been possible to make any sufficient
statements about the influence of using digestate as a fertilizer on
soil quality. The properties of this substance are decisively influ-
enced on the one hand by the anaerobic, microbial fermentation
process and on the other by the actual substrates used. Apart
from a reduction in the amounts of dry matter caused by the
decomposition of easily convertible organic matter (
), major changes to its properties include a higher NH
4
–N
∗ Corresponding author. Tel.: +49 345 5522603.
E-mail address:
barbara.koblenz@landw.uni-halle.de
(B. Koblenz).
concentration (
). In terms of its properties, therefore,
this type of fertilizer is considerably different from conventional
cattle and pig slurry.
As representatives of macrofauna, earthworms respond very
sensitively to various forms of land cultivation, which is why they
are used as an important bio-indicator when evaluating soil qual-
ity (
). Organic as well as chemical fertilizers serve
as a food source for earthworms, either directly or indirectly by
increasing crop and root residues. Fertilization is thus, also highly
important for earthworm activity in addition to tillage, pH value,
soil moisture and a site’s weather conditions. In many respects,
earthworms have important functions in the agricultural ecosys-
tem. For the most part this involves decomposing organic matter
as well as forming stable clay-humus complexes and the establish-
ment of a consistent macro-pore system.
Due to the rapid growth of biogas plants there is still a consider-
able lack of underlying data concerning the influence on earthworm
populations of fertilizing soil using digestate. So far there have
only been rudimentary attempts at comprehensively studying the
impact on earthworms – as a bio-indicator – of fertilizing soil using
http://dx.doi.org/10.1016/j.indcrop.2014.12.024
0926-6690/© 2014 Elsevier B.V. All rights reserved.
B. Koblenz et al. / Industrial Crops and Products 66 (2015) 206–209
207
Table 1
Main characteristics of cattle slurry and digestate used in the experiment in Cun-
nersdorf on a dry weight basis for cattle slurry and digestate respectively (idm = in
dry matter).
Cattle slurry
Digestate
Applied amount[m
3
]
86
Applied amount[m
3
]
70
Dry matter[%]
9.00
Dry matter[%]
4.90
Total nitrogen[%]
0.38 idm
Total nitrogen[%]
0.42 idm
NH
4
–N[%]
0.21 idm
NH
4
–N[%]
0.25 idm
digestate (
Ernst et al., 2008; Bermejo Domínguez, 2012
). In par-
ticular, it is still not possible to draw any conclusions about the
influence of fertilization with digestate on earthworms after a cou-
ple of years. Based on two field trials, this study aims to assess the
impact, both in the short term and over a three-year period, on
earthworms of applying fermentation residues to soil. The study
will also investigate and evaluate the influence of using digestate
as a fertilizer compared with using traditional slurry, chemical fer-
tilizers and an untreated control.
2. Materials and methods
2.1. Experimental site
2.1.1. Site 1 Cunnersdorf
The field trial in Cunnersdorf (Saxony, 12
◦
13’E, 51
◦
24’N) is
located in central Germany at 130–140 m AMSL. The predominant
soil texture in the topsoil is a silt loam (90 g kg
−1
clay, 330 g kg
−1
sand). In terms of soil typology, the test site can be classified
as a Stagnic Luvisol. Cunnersdorf has a mean annual temperature
of 8.9
◦
C (1977–2011) and mean annual precipitation of 619 mm
(1977–2011).
The experimental setup was a one-year, single-factor strip
design with four replicates. The crop grown was maize, and the
preceding crop was oat. In addition to an unfertilized control vari-
ant and a test element fertilized with mineral nitrogen only, the
trial investigated raw slurry and fermentation residues.
Before the experiment was set up, the land was ploughed to a
depth of approximately 25 cm. The slurry was spread on individual
test elements on 19.03.2009 using a special method to inject it at
a soil depth of approximately 10 cm. As the capacity of the trac-
tor’s slurry tank was not large enough for an entire test element,
each test element was driven over twice in immediate succession.
It was possible to place the second portion in precisely the area
that remained after application of the first portion. Approximately
86 m
3
of cattle slurry and 70 m
3
of digestate were spread in order
to meet nitrogen requirements of about 160 kg ha
−1
NH
4
–N. The
contents of the two agricultural fertilizers are shown in
digestate originated from a co-fermentation plant with a secondary
fermenter. In addition to cattle slurry, the biogas plant mainly fer-
ments maize. Earthworms were caught on 09.04.2009. The maize
was drilled five weeks after spreading the slurry (22.04.2009).
2.1.2. Site 2 Pfahlheim
The test site Pfahlheim is located 484 m AMSL in southern
Germany in the foothills of the Swabian Jura. The soil type is a Luvi-
sol. Based on the particle size composition, the soil texture in the Ap
horizon can be described as a silt loam (244 g kg
−1
clay, 146 g kg
−1
sand). On average this site has 840 mm of precipitation each year
as well as an annual average temperature of 7.7
◦
C.
The experiment was set up back in 2007 using a fully random-
ized, single-factor block design with four replications, and from the
very beginning conservation tillage was employed down to a soil
depth of 15 cm. The raw slurry and digestate were spread using drag
hoses on 23.04.2009. With 30 m
3
each of digestate and pig slurry,
130 kg N were spread per hectare. Next a tooth cultivator was used
Table 2
Main characteristics of pig slurry manure and digestate used in the experiment in
Pfahlheim on a fresh weight basis for pig slurry and digestate respectively (ifm = in
fresh matter).
Pig slurry
Digestate
Applied amount[m
3
]
30
Applied amount[m
3
]
30
pH value
8.3
pH value
8.6
Total nitrogen[%]
0.7 ifm
Total nitrogen[%]
0.8 ifm
NH
4
–N[%]
0.5 ifm
NH
4
–N[%]
0.5 ifm
to carefully incorporate the organic fertilizers into the ground. The
amount of chemical fertilizer used was equivalent to 165 kg N per
hectare; it was applied by adding two doses of calcium ammonium
nitrate (65/100 kg ha
−1
N). Using the experimental design of the
study presented here, the following test elements were examined
on 28.05.2009 during the third year of the experiment: ‘untreated
control variant’, ‘chemical fertilizer (calcium ammonium nitrate)’,
‘pig slurry’ and ‘digestate’.
The digestate used in the study came from a co-fermentation
plant. There was no secondary fermenter at the time of sampling.
The substrates used in this biogas plant include renewable raw
materials such as maize and grass silage as well as cereal grain.
Poultry dung is also fed into the biogas plant to be used as an
additional fermentation substrate. More information about the
properties of the organic fertilizers is listed in
2.2. Sampling and analysis
Earthworms were caught approximately four weeks after fertil-
ization (
) using a combination of hand-sorting
to a depth of 30 cm and a subsequent extraction of deeper living
earthworms by formaldehyde solution. By combining the etholog-
ical, active method of formalin extraction with the passive method
of hand-sorting, it is possible to significantly increase the effective-
ness of catching worms on arable land (
). The total
sampling area covered 1 m
2
; a metal ring 0.125 m
2
in size was used
to demarcate the border of the sampling area. Then a block of soil
approximately a spade deep was removed from the demarcated
area and searched for earthworms. Afterwards approximately 2 l of
a 0.2% formalin solution were poured into the hole in the ground.
Any earthworms that emerged were collected, washed in water for
approximately 20 min and preserved in jars of ethanol. The test was
performed with eight replicates per variant. The sampling areas
were selected in such a way that they proportionately contained
different aspects of one plot (row of maize and the space between
two rows of maize). Species identification followed
. For each variant the parameters ‘abundance’ [individuals
m
−2
], ‘biomass’ [g m
−2
] and ‘species dominance’ [%] were defined.
2.3. Statistical analyses
The earthworm abundance and biomass results between earth-
worm populations in each variant were statistically verified using
the distribution-free Mann-Whitney test (U-test) (
Significant values (p < 0.05) are represented by different letters.
3. Results
3.1. Site 1 Cunnersdorf
No significant differences in earthworm abundance and biomass
were observed in the variants with raw slurry and digestate at the
Cunnersdorf site (
). In these two organic fertilizers, signif-
icantly higher biomasses were identified in comparison with the
remaining variants. Overall abundance (adult and juvenile speci-
mens) was also higher in the test elements with raw slurry and
208
B. Koblenz et al. / Industrial Crops and Products 66 (2015) 206–209
Table 3
Influence of different treatments on earthworm numbers m
−2
and biomass (g m
−2
)
in Cunnersdorf, sampled on 09.04.2009. Different letters indicate significant differ-
ences between the treatments according to Mann–Whitney test (P < 0.05).
Treatment
Abundance
[indiv. fresh
weight m
−2
]
Earthworm
biomass [g m
−2
]
Control
Juvenile
35
12.76
Adult
11
7.87
Total
46
b
20.63
b
Mineral fertilizer
Juvenile
32
7.69
Adult
6
4.37
Total
38
b
12.06
b
Cattle slurry
Juvenile
72
21.69
Adult
14
15.42
Total
86
a
37.11
a
Digestate
Juvenile
62
18.05
Adult
14
11.22
Total
76
ab
29.27
a
Letters a and b indicate significant differences between the treatments.
Table 4
Influence of different treatments on earthworm numbers m
−2
and biomass (g m
−2
)
in Pfahlheim, sampled on 28.05.2009. Different letters indicate significant differ-
ences between the treatments according to Mann–Whitney test (P < 0.05).
Treatment
Abundance
[indiv. fresh
weight m
−2
]
Earthworm
biomass [g m
−2
]
Control
Juvenile
45
17.26
Adult
32
23.69
Total
77
a
40.95
a
Mineral fertilizer
Juvenile
21
7.50
Adult
22
23.50
Total
43
a
31.00
a
Pig slurry
Juvenile
26
9.45
Adult
31
36.69
Total
57
a
46.14
a
Digestate
Juvenile
27
12.57
Adult
33
31.56
Total
60
a
44.13
a
digestate. The variant with raw slurry (86 ind m
−2
) was the only one
to differ significantly from the unfertilized and chemical variants
(46 ind m
−2
and 38 ind m
−2
respectively). Compared with diges-
tate, there was a tendency for fertilization with unfermented slurry
to yield comparatively higher earthworm abundance and biomass.
The determination of age ranges resulted in far more juvenile earth-
worms than adults per square meter in all of the variants examined.
A total of four species were recorded (Aporrectodea caliginosa,
Aporrectodea rosea, Allolobophora chlorotica and Lumbricus ter-
restris) from three genera. The species A. caliginosa and L. terrestris
were present in all of the fertilization variants. Accounting for more
than 50% in each variant, the most dominant species was the min-
eral soil dweller A. caliginosa. As regards community composition
(
), spreading digestate points to a decrease in the endogeic
species A. rosea. Furthermore, the proportions of each ecological
group in the total population change. Evidence of the species A.
chlorotica is only present in the raw slurry variant. The species A.
caliginosa and L. terrestris are the only ones present in the digestate
variant.
3.2. Site 2 Pfahlheim
Earthworm abundance and biomass were examined in the vari-
ants ‘unfertilized’, ‘chemical’, ‘raw slurry’ and ‘digestate’. Overall
there are no statistically reliable differences between these vari-
ants.
At the Pfahlheim site, earthworm biomass tended to be higher in
the test elements with raw slurry and digestate than in the chem-
ical fertilizer and untreated variants (
). At 46.1 g m
−2
, the
test element with raw slurry displayed the greatest biomass. The
unfertilized variant returned the highest abundance, at 77 ind m
−2
.
This is attributable to the high number of A. rosea. The variants with
raw slurry and digestate had 57 and 60 ind m
−2
, respectively.
Analyzing the ecological groups, it can be seen that each vari-
ant contained mostly endogeic earthworms as well as one anecic
species in the form of L. terrestris. The absence of epigeic life forms
can be explained by the lack of leaf litter on arable land. Essentially
the species observed (A. caliginosa, Aporrectodea nocturna, A. rosea,
A. chlorotica and L. terrestris) are typical of arable land. The range of
species was the same in all of the variants investigated. However,
there were considerable differences in terms of dominance struc-
ture (
). There tended to be less individuals of the species
A. rosea observed in the variants with raw slurry and digestate. In
contrast, there were increased levels of A. caliginosa.
4. Discussion
In the field trials, the differentiation that occurred among
earthworm populations from various fertilization variants largely
confirms previous results from the literature, which show that an
organic fertilizer has a far more positive impact on earthworms
than a chemical fertilizer or an untreated control can (
and Lofty, 1982; Whalen et al., 1998
). Organic fertilizers provide earthworms with
an immediate, large supply of organic matter (
), while chemical fertilizers indirectly
supply organic matter more slowly in the form of crop and root
residues. At the Cunnersdorf site as well as Pfahlheim, there were no
statistically reliable differences between conventional slurry and
digestate when comparing earthworm abundance. Both organic
fertilizers had an equally positive influence on earthworm popula-
tion. In Pfahlheim, three years after the study began the earthworm
population tended to have been increased by both organic fer-
tilizers, although there are different. The raw slurry included pig
manure and the digestate based on poultry dung, maize, grass silage
and cereal corn which have an effect on several properties of the
organic fertilizers such as dry matter content and nutritional val-
ues. At the Cunnersdorf site, significant differences can be observed
between fertilization with slurry or digestate, on the one hand,
and using a chemical fertilizer or the untreated control on the
other. Our results are in agreement with the work of
, who also observed a larger earthworm population shortly
after applying organic matter. Despite all this, it is surprising that
in Cunnersdorf significant differences appeared between the dif-
ferent fertilization treatments just four weeks after fertilization.
Investigations by
do however indicate that fertil-
ization using a conventional slurry results in increased earthworm
biomass compared with fermented slurry. During the biogas pro-
duction process, the substrates’ readily soluble carbon bonds are
mostly broken down. Even so, in both experiments the digestate
did apparently provide improved nutritional quality and availabil-
ity for earthworms than was the case with chemical fertilizers and
the unfertilized control. The reasons for this seem to be related to
biogas plant technology. Especially in stirrer tank digesters, which
is where the digestate used in the field trials in Cunnersdorf and
Pfahlheim came from, the mixing process causes part of the fresh
substrate to end up in the outlet. This in turn provides soil fauna
with a food source in the form of readily degradable carbon com-
pounds. As digestate continues to be removed from the fermenter,
parts of the active biomass also continue to be discharged (
). While these anaerobic organisms do die immediately
after being deposited in the fermentation residue storage container,
they nevertheless offer earthworms an additional food source in
B. Koblenz et al. / Industrial Crops and Products 66 (2015) 206–209
209
Table 5
Community composition in numbers (%) in different fertilizer treatments at the study site Cunnersdorf (09.04.2009) and Pfahlheim (28.05.2009).
Species
Cunnersdorf
Pfahlheim
Control
(%)
Mineral fertilizer
(%)
Cattle slurry
(%)
Digestate
(%)
Control
(%)
Mineral fertilizer
(%)
Pig slurry
(%)
Digestate
(%)
Lumbricus
terrestris
9.1
33.3
14.3
7.1
6.3
18.2
16.1
12.1
Aporrectodea
caliginosa
81.8
50.0
57.1
92.9
25.0
22.7
64.5
63.6
Aporrectodea
rosea
9.1
16.7
14.3
–
53.1
22.7
3.2
3.0
Allolobophora
chlorotica
–
–
14.3
–
3.1
13.6
9.7
6.1
Aporrectodea
noctorna
–
–
–
–
12.5
22.8
6.5
15.2
the form of microbial protein. The relatively high number of earth-
worms in the unfertilized control in Pfahlheim seems to be that
earthworms have been negatively affected through the applica-
tion of both organic fertilizers. Some studies show these results
of slurry and digestate on earthworms (
Ernst et al., 2008; Bermejo Domínguez, 2012
). The negative effects
of slurry are related to its high salt concentration and the occur-
rence of substances that might be toxic to earthworms (
). In addition, the ammonia content may adversely affect soil
dwelling earthworms, especially in the digestate treatment. The
high abundances and biomass levels at the Cunnersdorf site might
be the result of earthworms having migrated. The experimental
setup allowed them to migrate to variants with a more attractive
food supply.
declare a natural spread rate
of between 2 and 15 m per year when earthworms colonise habitats
with more favorable living conditions.
The earthworm population in Cunnersdorf was characterised
by a high number of juvenile specimens. This might indicate a
higher reproduction rate. In terms of their dominance structure,
both of the sites examined are typical representatives of arable land
(
). At Cunnersdorf, applying digestate resulted in a
less varied range of species. Abundance of the endogeic earthworm
species A. rosea declines. This contradicts research by
, where something of a decrease in A caliginosa biomass was
observed after treatment with digestate. In the variant with diges-
tate, the most common species were A. caliginosa and L. terrestris.
As a primary decomposer, the anecic earthworm L. terrestris finds
sufficient food in this fertilization variant. The mineral soil dweller
A. caliginosa benefits from the higher feeding activity of L. terrestris
(
). Overall, the differentiation that occurred in the
field trials among earthworm populations from various fertiliza-
tion variants rather confirms previous results from the literature,
which show that an organic fertilizer has a far more positive impact
on earthworms than a chemical fertilizer or an untreated control
can (
Edwards and Lofty, 1982; Whalen et al., 1998
et al., 2006; Ulrich et al., 2010
Acknowledgements
We thank Prof. Niclas, Dr. Schuster, Dr. Kreuter and M. Fuchs
from SKW Stickstoffwerke Piesteritz GmbH as well as Dr. M. Mokry
and M. Müller from LTZ Augustenberg for allowing us to use their
study area in order to investigate this problem. A.-K. Schmitt, T.
Leithold and E. Koblenz are acknowledged for their support during
soil fauna sampling.
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