Ecological Indicators 117 (2020) 106586

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original Articles

Establishing reference values for soil microbial biomass-C in agroecosystems T

in the Atlantic Forest Biome in Southern Brazil
⁎
Raphael Antoine Anzalonea, Fabiane Machado Vezzania, , Glaciela Kaschuka,
Mariangela Hungriab, Luciano Kayser Vargasc, Marco Antonio Nogueirab
a
Departamento de Solos e Engenharia Agrícola, Universidade Federal do Paraná, Rua dos Funcionários, 1540, 80035-050, Curitiba, Paraná, Brazil
b
Embrapa Soja, CP 231, 86001-970 Londrina, Paraná, Brazil
c
Departamento de Diagnóstico e Pesquisa Agrícola, Secretaria da Agricultura, Pecuária e Irrigação, Rua Gonçalves Dias 570, Porto Alegre, Rio Grande do Sul, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: Soil microbial biomass plays a key role in the biogeochemical cycles, degradation of organic pollutants and soil
Bioindicator aggregation, and its estimation through soil microbial biomass-C (MB-C) is often referred as a potential indicator
Soil microbial biomass of soil functioning. This study aimed to identify reference values of MB-C that would relate to crop yield.
Soil monitoring Soybean and maize grain yields and microbial biomass-C (MB-C) data were gathered from studies listed in “Web
Crop yield
of Science” performed in agroecosystems located in the Atlantic Forest Biome in Southern Brazil. Database was
Meta-regression
Sustainability
composed by 78 datasets, where soil samplings for evaluation of MB-C were performed at the 0–10 cm layer at
Soybean flowering stage, and evaluated by the fumigation-extraction method. A meta-regression using the Mitscherlich
Maize model was applied to determine the MB-C reference value corresponding to 80% of maximum yield. The effects
of soil management systems and crop systems were verified by comparing the confidence intervals. Soil tillage
decreased MB-C and yield, while crop rotation increased yield but not MB-C. It was not possible to find a
reference value for soybean, because of the variability not explainable by the MB-C. The reference value related
to high maize yield (> 6,752 kg ha−1) was of 170 μg C g−1 soil, but further results must be included to decrease
the variability.

1. Introduction conditions such as soil compaction, salinity and acidity (Egamberdieva

One agroecosystem comprises a set of biotic (plants, animals, mi-
croorganisms) and abiotic (minerals, topography, air, humidity, tem-
perature, luminosity) components organized in a complex system spe-
cialized and controlled to provide agricultural production (Okey,
1996). The maintenance of the agroecosystem’s functions, including
biogeochemical cycles, population regulation, among others, depends
on the diversity and relationship between its components (Altieri,
1999), which in turn, are highly dependent on the soil capacity to
sustain all living organisms.
Soil is the habitat of a great diversity of microorganisms (fungi,
bacteria, algae, archaea and protozoa) (Lankau and Keymer, 2018;
Porazinska et al., 2012), which compose the soil microbial biomass. Soil
microbial biomass is usually estimated on basis of its C content, and
referred as microbial biomass-C (MB-C) (Jenkinson and Powlson, 1976;
Vance et al., 1987). The MB-C depends on the availability of plant re-
sidues, that contain organic C and other nutrients, such as N, P, S and
micronutrients (in ‘t Zandt et al., 2018) and is affected by adverse
et al., 2010; Pietri and Brookes, 2009; Šantrůčková et al., 1993) and
other processes like intensive tillage . The microorganisms play a key
role in nutrient cycling and degradation of pollutants, since they are the
central agent of soil organic matter degradation (Dalal, 1998). As mi-
croorganisms exude organic compounds, they also contribute to the
formation and stabilization of soil microaggregates (Degens, 1997;
Lehmann et al., 2017; Panettieri et al., 2017; Rillig, 2004). Their eco-
logical interactions by symbioses, parasitism and predation contribute
to the regulation of populations and biological control of plant diseases.
As both crops and microorganisms compose the same agroeco-
system, they depend on each other to maintain mutual support. Several
studies aiming to identify soil properties indicative of agroecosystem
functioning or soil quality have proposed MB-C as a consistent micro-
biological indicator; another advantage is its low operational costs for
routine analyses (Kaschuk et al., 2010, 2011; Askari and Holden, 2014;
Coser et al., 2016; da Freddi et al., 2017; Granatstein and Bezdicek,
1992; Guimarães et al., 2017; Lopes et al., 2018). In general, MB-C data
from agroecosystems are compared with MB-C of reference sites, either

⁎
Corresponding author.
E-mail address: vezzani@ufpr.br (F. Machado Vezzani).

https://doi.org/10.1016/j.ecolind.2020.106586
Received 8 March 2019; Received in revised form 5 May 2020; Accepted 28 May 2020
1470-160X/ © 2020 Elsevier Ltd. All rights reserved.
R.A. Anzalone, et al.
agricultural or natural (Barbosa et al., 2017; Kaschuk et al., 2011;
Sattolo et al., 2017; Silva et al., 2010). However, undisturbed systems
have often a lower agronomic potential and their MB-C in general is
considerably higher, thus such comparison is not useful to identifying a
characteristic level of a functioning soil.
Considering the limitation of using MB-C values of undisturbed
areas as reference, the objective of our study was to establish MB-C
reference values based on the relationship between BM-C and soybean
and maize yield and reference values in the Atlantic Forest biome in
Southern Brazil.
2. Material and methods
2.1. Data collection
Data collection started by browsing the “Web of Science” for articles
that contained the key-words “soil microbial biomass” and applying a
filter to select only articles related to Brazil, resulting in a list of 716
articles. Every article was thoroughly checked and only those fulfilling
the following criteria were maintained for further analyses: 1) contain
information on both MB-C and crop yield; 2) report experiments per-
formed in Brazil with commonly cultivated crops; 3) report measure-
ments from agroecosystems managed for at least three years; 4) pub-
lished between 1996 and 2016; and, 5) the study aiming at the
evaluation of the agroecosystems, not the effects of pollutants or in-
dustrial residues. The collection totaled 652 datasets (a dataset re-
presents a plot in a given experiment simultaneously containing data on
MB-C, yield, etc).
Since the data were obtained from different studies, there was high
heterogeneity, according to geographic conditions (Fig. 1 a, b, c), soil
types (Fig. 1 d, e), management (Fig. 1 f, g, h), plant growth stage, soil
sampling depth (Fig. 1 i, j) and methodology for MB-C assessment
(Fig. 1 k). Before the high heterogeneity observed, we decided to re-
strict the datasets to those related to the conditions mostly represented
in the collection to run the following statistical analysis such as: 1)
experimental areas located in the Atlantic Forest biome, all of them
situated in Southern Brazil (predominantly in Paraná State); 2) yields of
soybean (Glycine max L. Merrill) and maize (Zea mays L.); 3) soil
sampling at flowering stage in the 0–10 cm layer; 4) evaluation by the
fumigation-extraction method. The latter restriction criteria resulted in
78 datasets from agroecosystems characterized by clayly soils classified
as Oxisols (421–720 g clay kg−1) [Latossolos, in Brazilian Soil Classi-
fication System (Santos et al., 2018)], located in Cfa or Cfb climates.
2.2. Comparisons between management systems
The management systems studied were soil tillage systems: no-til-
lage (planting in a narrow trench, without soil tillage); minimum tillage
(soil mobilization up to 15 cm, without plowing); conventional tillage
(soil plowing or disking and a second soil mobilization) and cropping
systems: succession (sequence of more than one crop during the year,
repeated yearly) and rotation (sequence of more than one crop on at
least two years). A confidence interval (significance level of 0.05) for
MB-C and yield of soybean and maize was determined for each man-
agement system using the meta-analysis random effects model
(Kulinskaya et al., 2008). Differences between the management systems
were considered significant when the confidence intervals did not
overlap.
2.3. Determination of the soil microbial biomass (MB-C) reference value
The determination of the reference value for MB-C (MB-Cref) was
performed using the Mitscherlich equation. This mathematical model is
indicated to describe a phenomenon with plateau, representing the
mathematical relation between a response variable that tends to a
maximum with the increase of an input variable. In this case, the crop
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Ecological Indicators 117 (2020) 106586
yield was used as response variable as function of the MB-C, as shown in
Eq. (1).
Y = Ymax . (1 − e−b . MB − C ) (1)
−1
where, Y is the yield (kg ha ) of soybean or maize; soil microbial
biomass is represented by the MB-C (μg C g−1), Ymax represents the
maximum yield (kg ha−1); and b is the parameter that indicates the
quickness of the model to hang over the plateau. The model was applied
individually for soybean and maize, due to the difference between the
yield levels of the two crops. The values of the parameters Ymax and b
were determined using the nonlinear regression function nls of the
statistical software R (R Core Team, 2016)). The weight given to each
observation was inversely proportional to the standard deviation. When
the standard deviation was not reported, it was calculated considering a
coefficient of variation two-fold higher than the average coefficient of
variation of the other datasets.
For the MB-Cref, we considered a MB-C referring to 80% of max-
imum yield, as suggested before (Lopes et al., 2013), and the value was
obtained from Eq.(2):
ln(0, 2)
MB − Cref =
b (2)
where b is the parameter determined by the Eq. (1).
3. Results and discussion
3.1. Are soil microbial biomass (MB-C) and soybean and maize yields
sensitive to tillage in soils of the Brazilian Atlantic Forest biome?
The MB-C of agricultural areas of the Atlantic Forest biome of
Southern Brazil assessed at soybean flowering presented lower values
under conventional tillage (CT) and minimum tillage (MT) in compar-
ison with no-tillage (NT) (Fig. 2a). This can be attributed to the de-
crease in soil organic matter (SOM) induced by the soil disturbance,
which leads to the disruption of the aggregates and exposing the SOM
to microbial oxidation (Blanco-Moure et al., 2016). For the maize da-
taset, we observed no effect of tillage on MB-C (Fig. 2 a). Although
negative effects of tillage on the MB-C have been often reported (e.g.
Kaschuk et al. 2010; 2011), other sources of variability, such as clay
content or sampling time can mask this trend (Hungria et al., 2009;
Venzke et al., 2008).
Decreases in yield under CT in relation to NT system were observed
for the soybean (9%) and maize (11%) (Fig. 2b). Although there may
have some controversy in relation to the benefits of NT on crop yields
(e.g. Giller et al., 2009; Pittelkow et al., 2015), in South America the
improvements are well documented, resulting in impressive crop yields
(Derpsch et al., 2010). Soil tillage may increase crop yield increases in
the short-term (Santos et al., 2007) because disking and ploughing can
momentarily correct soil physical conditions and lead to a rapid mi-
neralization of SOM (Stone et al., 2013; Tivet et al., 2013), providing
nutrients, mainly N, P and S for plant growth. However, with time, as
SOM decreases, soil aggregates are disrupted, leading to unfavorable
physical and fertility properties (e.g. Hungria et al., 2009; Kaschuk
et al., 2010).
3.2. How sensitive are soil microbial biomass and soybean yield to cropping
systems?
The relationship between MB-C and yield in different cropping
systems (crop rotation or succession) is shown in Fig. 3 only for soybean
because the dataset related to maize was too little for this type of
analysis. The MB-C in soybean-cropped soils did not differ between
cropping systems. Cropping systems including legumes would promote
the MB-C (Hungria et al., 2009; Pereira et al., 2007; Silva et al., 2010).
However, the effects of cropping systems on MB-C are more likely to be
associated with previous crop that leave greater amounts of residues
R.A. Anzalone, et al. Ecological Indicators 117 (2020) 106586

(caption on next page)

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R.A. Anzalone, et al. Ecological Indicators 117 (2020) 106586

Fig. 1. Data distribution in a) Brazilian states, b) biomes, c) climate, d) soil sub-orders according to the Brazilian Soil Classification System, e) soil textural classes, f)
soil management systems, g) crop sistems, h) crops at soil sampling time, i) crop growth stage at soil sampling, j) soil depth sampling, k) soil microbial biomass
quantification method. * PVA: Argissolo Vermelho-Amarelo (Ultisol); PV: Argissolo Vermelho (Ultisol); CX: Cambissolo Háplico (Inceptisol) LV: Latossolo Vermelho
(Oxisol); LVA: Latossolo Vermelho-Amarelo (Oxisol); n.a.: data not available. *** Cumulated yield of maize and soybean. ** Composition of mixed crop systems:
maize (Zea mays L.) + velvet bean (Mucuna spp.)/lettuce (Lactuca sativa L.) (n = 18), bean (Phaselous vulgaris L.) + crotalaria (Crotalaria spp.)/maize + crotalaria
(n = 8), bean + pigeon pea (Cajanus cajan L. Millsp.)/maize + pigeon pea (n = 8), bean + velvet bean/maize + velvet bean (n = 8), bean + sorghum (Sorghum
bicolor L., Moench)/maize + sorghum (n = 8). Composition of rotations: soybean (Glycine max L. Merrill)/wheat (Triticum aestivum L.)/white lupin (Lupinus albus
L.)/maize/black oat (Avena strigosa Schreb.)/fodder raddish (Brassica rapa L.) (n = 36), maize/pearl millet (Pennisetum glaucum (L.) R.Br.)/soybean/pearl millet
(n = 24), black oat/maize/black oat/soybean (n = 22), soybean/maize (n = 18), soybean/wheat/maize/black oat (n = 18), other rotations (n = 102). Composition
of succession: soybean/maize (n = 58), soybean/wheat (n = 33), bean/maize (n = 23), maize/lettuce (n = 18), soybean black oat (n = 7), other successions
(n = 10).

(i.e. maize produces more biomass than soybean) (Balota et al., 2004,
1998). Therefore, if we consider the soil MB-C as a biological indicator
of soil functioning and relate it to sustainable crop systems, we may
foresee that cropping systems should only increase species richness over
time (as in rotation system), but also increase the quantity and quality
of residues (e.g. Shahbaz et al., 2017).
The crop rotation system increased soybean yield compared with
the crop succession system (Fig. 3b). This increase may be, among
several causes, a consequence of diversified crops, which decreases the
potential inoculum of pathogens (Hossard et al., 2017) and reduces
phytosanitary problems (Pankhurst et al., 2002; Young et al., 1986).
The yield increase under crop rotation can also be explained by a more
efficient use of nutrients due to the complementarity of root archi-
tecture of the different crops involved in the rotation and their re-
spective absorption capacities (Agegnehu et al., 2014).
3.3. What is the reference value for MB-C in agroecosystems of the Atlantic
Forest biome in Southern Brazil?
Modelling evidenced that soybean yield was highly variable and
could not be explained by the MB-C (Fig. 4a) even though there were
concomitant increases in MB-C and yields in individual experimental
areas (Cervantes, 2012; Garbuio, 2009; Hungria et al., 2009; Silva et al.,
2010). However, it should be considered that soybean yields in the
dataset remained above 3,300 kg ha−1, above the Brazilian average in
the period (2,900 kg ha−1; Moreira, 2017), even at the lowest values of
MB-C (below 200 μg C g−1; Fig. 4a). Under conditions of Brazilian
Cerrado where MB-C generally is lower than in Atlantic Forest (Kaschuk
et al., 2010). Figueiredo (2009) found MB-C between 150 and 250 μg C
g−1 (i.e. relatively low values), in agroecosystems with soybean yield
above 3,000 kg ha−1, the regional average of the Brazilian Midwest in
2010 (CONAB, 2013).

a)
NT ns n = 17
Maize

CT ns n = 9

NT a n = 25

MT b n=7
Soybean

CT b n = 17

0 100 200 300 400 500 600

Soil microbial biomass (μgC g-1soil)

b)
NT a n = 17
Maize

CT b n=9

NT a n = 25

MT ab n = 7
Soybean

CT b n = 17

0 1000 2000 3000 4000 5000 6000 7000 8000 9000 10000
Grain yield (kg ha-1)

Fig. 2. Soil microbial biomass (a) and yield (b) relate to soil management system for soybean and maize crops. Error bars represent confidence interval (α = 5%).
Treatments followed by the same letter do not differ. ns: no significative difference. NT: no-tillage, MT: minimum tillage, CT: conventional tillage.

4
R.A. Anzalone, et al.
Rotation
Succession
0 100 200
Rotation
Succession
0 500 1000
Fig. 3. Soil microbial biomass (a) and yield (b) relate to crop system for soybean crop. Error bars represent confidence interval (α = 5%). Treatments followed by the
same letter do not differ. ns: no significative difference.
The values of MB-C and maize yield fitted well with the Mitscherlich
model (Fig. 4b; p < 0.001). The asymptote representing the predicted
maximum yield was 8,440 kg ha−1. If the threshold of 80% of max-
imum yield was used to consider high yield (i.e. 6,752 kg ha−1), the
corresponding reference value for MB-C was 170 μg C g−1 (Fig. 4b).
Thus, for MB-C lower than 170 μg C g−1 yields lower than 80% of
maximum yield should be expected. However, in our modelling, there
was no observation below 200 μg C g−1 (Fig. 4b).
By using a quadratic regression between MB-C and cumulative
yields of soybean and maize for 18 years, Lopes et al. (2013) estimated
the reference value of MB-C in a clayey soils of the Brazilian Cerrado
biome as 375 μg C g−1. In that case, 55% of the treatments that had MB-
C between 290 and 375 μg C g−1 were related to yields corresponding
to 89 to 100% of maximum yields, whereas above 375 μg C g−1, 87% of
the treatments presented cumulative yield higher than 80% of max-
imum accumulated yield.
3.4. Yield, agroecosystem productive capacity and soil microbial biomass
From the results of this work and in others (Lopes et al., 2018,
2013), it was possible to propose three MB-C intervals in relation to
crop yield (Fig. 5). The first one should be characterized by a low MB-C
and a low crop yield, from now named “compromised yield”. The
second presented a medium MB-C and a variable yield, named “high
yield possible”. Finally, the third was characterized by high MB-C and
high yield, named “guaranteed yield”. These three intervals correspond
to three types of agroecosystems: “degraded”, “dependent” and “sus-
tainable” (Fig. 5).
The “degraded” agroecosystem has low MB-C and low yield because
the soil functionality is hardly compromised. The limitations may be
related to soil compaction, inadequate to root growth and movement of
gases and water in the soil, in addition to possible nutritional defi-
ciencies, or any environmental factor that affects MB-C and crop yield
simultaneously. As plant growth is affected, the volume of plant bio-
mass production and its deposition to the soil is reduced. Thus, the
stock and flow of organic matter in the soil is low, limiting the micro-
bial biomass and activity responsible for the improvement of soil con-
ditions, thus maintaining the state of degradation of the agroecosystem
(Fig. 5). Along these lines, we propose a critical value to separate de-
graded from dependent agroecosystems.
Above the MB-C critical value and up to the sustainable value, the
agroecosystem enters a condition named as “dependent” agroecosystem
Ecological Indicators 117 (2020) 106586
ns n = 18
ns n = 33
300 400 500 600
Soil microbial biomass (μgC g-1soil)
a n = 18
b n = 33
1500 2000 2500 3000 3500 4000
Grain yield (kg ha-1)
(Fig. 5). In this condition, the agroecosystem depends on soil correction
by soluble fertilizer inputs to maintain a stock of nutrients readily
available for the plants, and/or soil tillage to achieve high yield. In this
agroecosystem, soil organic matter and biological activity are too poor
to promote a sufficient natural functioning to maintain soil in ideal
conditions for crops growth and development and, therefore, does not
have a proper productive capacity to support high crop yields (Vezzani
and Mielniczuk, 2009; Kaschuk et al., 2010). High yield can be possible
if correction practices are applied. Thus, this agroecosystem can be
productive, but it is not an ideal agroecosystem, since it depends on
constant fertilization and management actions, that are unsustainable
in the long term, considering the limitation of fertilizer stocks and en-
ergy sources (Cordell et al., 2009).
Above the sustainable value, the soil functions are fulfilled by the
edaphic biota, characterizing a “sustainable” agroecosystem, which has
its own high productive capacity. Thus, the high yield is more likely,
since the agroecosystem does not need constant soil correction. The
productive capacity is ensured because the microbiota fulfills the eco-
system functions necessary to naturally maintain soil attributes at ideal
levels, allowing the crop to reach high yields. This is because the mi-
crobial biomass works as source of nutrients temporally immobilized
and easily mineralizable to release nutrients (Coppens et al., 2006; Hu
et al., 2009; Ryan et al., 2006). In addition, the microbial community
also acts on the mineralization of pesticides (Jing et al., 2017; Lancaster
et al., 2010), and participate to bind soil particles, forming and stabi-
lizing soil aggregates (Fokom et al., 2012; Purin and Rillig, 2007). This
state is maintained by the generation a satisfactory amount of plant
biomass and management to maintain the energy and carbon supply for
the microbiota over time. The agroecosystem depends on an appro-
priate management that guarantees an input of organic carbon to the
soil, the maintenance of the structure and the sufficiency of nutrients to
remain in a favorable functioning condition.
In agroecosystems, the harvest leads to the exportation of nutrients
decreasing the agroecosystem productive capacity. Therefore, sustain-
able agroecosystem requires replacement of exported nutrients to
maintain the stock of nutrients contained in soil organic matter and
microbial biomass that will be the source of nutrients for future crops.
Dependent and degraded agroecosystems, in turn, require quick-release
fertilizers to supply the immediate demand of the crop for nutrients, but
also show a higher rate of loss of nutrients because they do not contain
sufficient soil organic matter and microbial biomass, which are able to
immobilize or retain nutrients temporarily (Figueiredo et al., 2007;
5
R.A. Anzalone, et al.
a)
b)
Fig. 4. Relationship between yield and soil microbial biomass in Atlantic Forest biome of in Southern Brazil. a) in soybean crop. b) in maize crop, using the
Mitscherlich relation and calculated soil microbial biomass reference value. The point diameter is inversely proportional to the standard deviation ***: p-
value < 0,001.
Varela et al., 2017).
In the present study, the reference value calculated from corn yield
(Fig. 4b) in highly managed and corrected experimental agroecosys-
tems was 170 μg C g−1, thus suggested as the MC-B critical value for
soils of the Atlantic Forest biome in Southern Brazil. Losses of pro-
ductive capacity of agroecosystems were not identified and no sus-
tainable value was found due to the lack of records of less corrected
agroecosystems in this region.
4. Conclusions
Considering the limitations of the model, the agroecosystems in the
Atlantic Forest biome in Southern Brazil (Paraná and Santa Catarina
States) with microbial biomass above 170 μg C g−1 are capable to
sustain high crop yields. Agroecosystems under soil tillage have lower
6
Ecological Indicators 117 (2020) 106586
soil MB-C and a lower crop yield than long-term no-tillage systems,
whereas agroecosystems that include crop rotations have greater crop
yields despite no increase in soil MB-C.
The conceptual model proposed in this study may be applied to
agroecosystems worldwide, but numeral thresholds are specific for the
Atlantic Forest Biome.
Credit authorship contribution statement
Raphael Antoine Anzalone: Conceptualization, Methodology,
Investigation, Formal analysis, Writing - original draft, Writing - review
& editing. Fabiane Machado Vezzani: Conceptualization, Supervision,
Writing - original draft, Writing - review & editing. Glaciela Kaschuk:
Conceptualization, Investigation, Writing - original draft, Writing - re-
view & editing. Mariangela Hungria: Conceptualization, Investigation,
R.A. Anzalone, et al.
Adequate management of soil organic matter
Inadequate management of soil organic matter, soil erosion
SMB critical value SMB reference value
Atlantic Forest (this study): 170 g C g-1soil
Yield Cerrado (Lopes et al., 2013): 290 g C g-1soil
Degraded Dependent agroecosystem
agroecosystem
Impracticable high High yield attainable if soil
yield condition correction
Fig. 5. Model of productive capacity, yield and the effects of soil management in agroecosystem from the point of view of soil microbial biomass. .
Adapted from Kaschuk et al. (2010)
Writing - review & editing. Luciano Kayser Vargas: Conceptualization,
Investigation, Writing - review & editing. Marco Antonio Nogueira:
Conceptualization, Investigation, Writing - review & editing.
Acknowledgments
The authors thank Jessica de Souza Pereira, Tatiana Suzin Lazeris
and Raul Matias Cezar for fruitful discussions about soil quality in an
earlier version of the manuscript; to Denise De Conti; Raphael Anzalone
received scholarship from the Coordination of Improvement of Higher
Education Personnel (CAPES, Brazil).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.ecolind.2020.106586.
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