Pedobiologia - Journal of Soil Ecology 78 (2020) 150607

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Pedobiologia - Journal of Soil Ecology

journal homepage: www.elsevier.com/locate/pedobi

Impact of exotic pastures on epigeic arthropod diversity and contribution of T

native and exotic plant sources to their diet in the central Brazilian savanna
Vinicius Tirelli Pompermaier*, Tiago Borges Kisaka, Juliana Fernandes Ribeiro,
Gabriela Bielefeld Nardoto
Departamento de Ecologia, Universidade de Brasília, Brasília, Brazil

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

Keywords: Much of the Brazilian savanna (known locally as the Cerrado) has been converted to pasture of African C4
Neotropical savannas grasses (exotic pastures) for livestock production. The resulting habitat simplification and decreased resource
Exotic grass availability may be significant factors underlying the impact on some soil arthropod groups, although it is still
Diversity loss unclear how the different soil groups respond to this impact in the Brazilian savanna. We sampled epigeic
Invertebrates
arthropods in exotic pastures, adjacent woodland savanna fragments (cerrado sensu stricto), and savanna-pasture
Stable isotopes
Mixing model
boundaries to investigate the impact of pasture on their diversity and activity, identifying the arthropods that
contribute most to the between-habitat dissimilarities and those most vulnerable to pasture implementation. We
also estimated the contribution of native and exotic plants to the diets of frequently observed arthropods in each
habitat using carbon and nitrogen stable isotope analysis. We found lower richness and diversity of epigeic
arthropods in pastures, where we also observed decreased activity of predator groups, whereas the activity of
Symphypleona and Poduromorpha springtails increased. Springtail orders and Myrmicinae morphospecies were
the main contributors to the between-habitat dissimilarities. Staphylinidae, Ptiliidae, and Zodariidae mor-
phospecies seem to be vulnerable to exotic pastures. Our isotopic models show that woodland savanna ar-
thropods feed preferentially on native C3-plant sources, while also showing signs of exotic C4 sources in their
diet. These outcomes indicate that foraging or dispersal events may occur between habitats since arthropods
captured in pastures also show signs of native sources in their diet.

1. Introduction
The Brazilian savanna (Cerrado) stands out as one of the most di-
verse tropical biomes, with the richest savanna in plant species of the
world and covering approximately 22 % of the Brazilian territory
(Oliveira and Marquis, 2002). Due to the high degree of species en-
demism and the rapid habitat loss through intense land use and slash-
and-burn practices, the Brazilian savanna is considered one of the 34
biodiversity hotspots in the world (Mittermeier et al., 2011). Approxi-
mately 56 % of the total land appropriated for intensive agriculture in
the Brazilian savanna has already been converted to human use. In
particular, pastures planted with African C4 grasses account for 68 % of
the anthropic land cover, occupying more than 25 % of the Brazilian
savanna (Sano et al., 2010). Many of these pastures are growing
alongside “cerrado sensu stricto” vegetation (woodland savanna), a
heterogeneous habitat composed of a shrub and arboreal strata domi-
nated by C3 plant species, and an herbaceous layer consisting of both
C3 and C4 grasses (Klink and Joly, 1989). Consequently, the cultivation
of pastures with only exotic C4 grasses imposes a less diverse and
complex habitat on the woodland savanna biota, with a different
quantity and quality of available resources. Together with changes in
soil attributes, these factors may impact ecosystem processes by food
web changes, beginning with the soil microbial community (Quirino
et al., 2009; Viana et al., 2011).
There is a growing concern about the impact that global environ-
mental changes already have and will probably have on soils, since they
harbor enormous organism diversity (Decaëns, 2010; Fierer et al.,
2009), which is responsible for key ecosystem functioning processes,
such as organic matter decomposition and nutrient cycling (Nielsen
et al., 2011). Evidence shows that loss of soil microorganism biodi-
versity impacts the ecosystem multifunctionality (Wagg et al., 2014).
However, it is still not clear if soil fauna diversity loss also has the same
effect, especially in the tropics, where knowledge about this biodi-
versity remains limited. What is known more clearly is that arthropods,

⁎
Corresponding author at: Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, 70919-900, Brasília, DF, Brazil.
E-mail addresses: pomper.official@gmail.com, pompermaier.vt@aluno.unb.br (V.T. Pompermaier), tiagobk.df@gmail.com (T.B. Kisaka),
jufernandesribeiro@gmail.com (J.F. Ribeiro), gbnardoto@unb.br (G.B. Nardoto).

https://doi.org/10.1016/j.pedobi.2019.150607
Received 11 January 2019; Received in revised form 29 October 2019; Accepted 21 November 2019
0031-4056/ © 2019 Elsevier GmbH. All rights reserved.
V.T. Pompermaier, et al.
which comprise a considerable portion of the soil meso and macro-
fauna, are notably affected by land use changes, decreasing in richness
and abundance in response to intensified management practices
(Attwood et al., 2008). In Brazilian ecosystems, even the conversion of
native vegetation to less intensive management systems like pastures
affects soil fauna composition and abundance in the forest (Barros et al.,
2006) and savanna ecosystems (Benito et al., 2004; Luz et al., 2013;
Marchão et al., 2009).
However, it is still unclear how the different soil arthropod groups
respond to exotic pastures in the woodland savannas, especially those
belonging to the mesofauna. Studies have shown that soil macrofauna
populations are totally or partially destroyed in the initial conversion of
the savanna to exotic pasture, and over time, recolonization is suc-
cessful only for groups able to consume and adapt to the new resources
(Benito et al., 2004). Arthropod populations in the remnant natural
fragments may also be impaired by the decrases in patch area (Hunter,
2002), but this aspect has not been investigated in the Brazilian sa-
vannas. A recurrent observation in exotic pastures implemented in
woodland savanna areas is the reduction of arthropod richness and
predator populations (Benito et al., 2004; Franco et al., 2016; Marchão
et al., 2009). For termites, one of the most representative groups in the
Brazilian savanna, the habitat simplification promoted by exotic pas-
tures through the partial or total removal of trees and shrubs negatively
affects xylophagous termites and positively affects grass-feeder termites
(Carrijo et al., 2009; Oliveira et al., 2013). This statement reveals that
we can better understand the impact of exotic pasture on savanna ar-
thropods if we better identify their trophic relationships with the
available resources.
This study aimed to investigate how exotic pastures impact the
epigeic arthropod community of Brazilian woodland savannas. We
hypothesized that exotic pastures would have a distinct arthropod
community structure, with lower species richness, diversity, and ac-
tivity-density compared with adjacent woodland savannas and sa-
vanna-pasture boundaries. In this sense, we seek to identify the groups
that most contribute to the between-habitat dissimilarity and those
most vulnerable to exotic pastures. We modeled the community data to
also include the patch area effect to test if the habitat type is the main
factor explaining arthropod community changes. Finally, we used
stable isotope analyses of carbon and nitrogen to evaluate the impact of
exotic pastures on epigeic arthropod diet by quantifying the proportion
of native and exotic plant sources consumed by them in each habitat
type.
2. Materials and methods
2.1. Study area
We conducted the study in two rural areas, both located in the
Ribeirão Mestre D’Armas region, a sub-basin of the São Bartolomeu
river basin, northeast Federal District, Brazil (15°35′54.11″ S and
47°45′02.89″ W). The altitude is approximately 1100 m, and the region
has a marked seasonality with dry winters and rainy summers. The
annual average precipitation is around 1500 mm, with summer rains
from October to March. At the peak of the dry season, the relative
humidity can be below 20 %. The mean annual temperature ranges
from 20 °C to 26 °C.
We selected the rural areas considering the same parent material,
geomorphologic compartment, and land cover as standardization cri-
teria (Pinheiro-Alves et al., 2016). In the areas, we selected three sites
on a plateau with clayey Oxisols covered by woodland savanna frag-
ments surrounded by adjacent exotic pastures (Fig. S1). The three sites
were more than 1 km apart from each other. The exotic pastures had
similar histories and consisted of small areas converted approximately
30 years ago, with about ten years of rotational cattle grazing under
low-intensity management with African C4 grasses. The exotic pastures
in site 1 and site 2 are grazed more frequently than the site 3 pasture,
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Pedobiologia - Journal of Soil Ecology 78 (2020) 150607
which is grazed twice per year, two months at a time, remaining fallow
the rest of the time. During the sampling period, all pastures were
fallow.
2.2. Sampling design
The sampling design consisted of three sites, each containing one
replicate plot for each of the following three habitats: woodland sa-
vannas, exotic pastures (growing with African grasses) and savanna-
pasture boundaries. Hereafter we will refer to the habitats only as sa-
vanna, boundary, and pasture. We delimited each savanna and pasture
area polygon using QGIS (version 2.12.3) to calculate its geometric
center. Savannas measured 19 ha (plot 1), 115 ha (plot 2), and 126 ha
(plot 3). Pastures measured 35 ha (plot 1) 9 ha (plot 2), and 17 ha (plot
3). With the aid of GPS, we established a sampling point in the geo-
metric center of each savanna and pasture area and another four points
15 m from the central point following a cardinal orientation. At the
boundaries, three points were aligned 15 m from each other in the sa-
vanna and pasture transition zone, and two points were entered 15 m
into each habitat. The boundary sampling points were more than 100 m
from the savanna and pasture sampling points. This nested sampling
design was considered in the analyses since the sampling points are not
independent (Fig. S1).
2.3. Epigeic arthropod sampling
We sampled epigeic arthropods from January to March 2015 (rainy
season) using pitfall traps (plastic pots 14 cm in diameter and 10 cm
deep). We buried one trap at ground level at each sampling point (five
traps in each replicate plot). We filled the traps with 70 % ethanol and
protected them from the rain with styrofoam plates placed above them
and fixed to the ground with wooden sticks. We removed the traps
seven days later.
We counted the arthropods using a stereomicroscope (magnification
up to 40×). Arthropods (belonging to macrofauna and mesofauna)
were identified based on the literature at the class and order levels, and
when possible, at the family and subfamily levels (Baccaro et al., 2015;
Brescovit et al., 2002; Krantz and Walter, 2009; Rafael et al., 2012;
Triplehorn and Johnson, 2005). Individuals of three groups generally
well represented in pitfall traps (Araneae, Coleoptera, and Formicidae)
were separated into morphospecies to improve the analyses of com-
munity structure and stable isotope ratios (Table S1). We identified the
morphospecies by a thorough morphological comparison, in that if we
mistakenly joined or separated the specimens, we assume this error is
standardized. We enlisted help from a specialist to support our se-
paration of the spider morphospecies. We grouped the Insect larvae at
the class level. We excluded from our analyses any orders represented
by a single captured individual (Ixodida and Phasmatodea), groups
whose main locomotion method is flight (e.g., Diptera), and those not
well represented by the sampling technique such as Hymenoptera
(other than Formicidae and Platygastroidea parasitoid wasps), Auche-
norrhyncha, and Lepidoptera adults.
2.4. Sample preparation for stable isotope analysis
Carbon and nitrogen stable isotope ratios were determined only for
some taxonomic groups (among orders and morphospecies) that in-
dividually or collectively reached a minimum weight (1.0 mg) to
compose a sample. Some well representative groups, such as beetles
and ants, and savanna and boundary arthropods had more replicate
samples per group. Overall, 52 samples of the savannas (belonging to
27 taxonomic groups and their replicates), 42 from the boundaries
(belonging to 30 groups and their replicates) and 26 from the pastures
(belonging to 19 groups and their replicates) were analyzed (Table S2).
We oven-dried the arthropods at 60 °C for 24 h and homogenized each
sample with an agate mortar and pestle. We then transferred samples
V.T. Pompermaier, et al.
from each taxon to small tin capsules until they weighed 1.0–2 mg.
The carbon and nitrogen isotope ratios were determined by com-
bustion using an elemental analyzer (Carlo Erba, CHN-1100) coupled to
a Thermo Finnigan Delta Plus mass spectrometer at the Laboratory of
Isotope Ecology of the Center for Nuclear Energy in Agriculture (Centro
de Energia Nuclear na Agricultura - CENA), University of São Paulo
(Universidade de São Paulo), Piracicaba, Brazil. The results were ex-
pressed in delta notation (δ), in parts per thousand (‰), based on an
internationally recognized standard. We used the following equation:
δ15N or δ13C (‰) = (RSample – RStandard) / RStandard × 1.000
where RSample and RStandard represent the heavy/light isotope molar
ratio of the sample and standard, respectively. The standard used for
carbon analysis was Pee Dee Belemnite (Vienna PDB; 13C:12C
ratio = 0.01118), and the standard used for nitrogen analysis was at-
mospheric air (15N:14N ratio = 0.0036765). The analytical error ob-
tained by the laboratory internal standard analysis was 0.3‰ and 0.5‰
for carbon and nitrogen, respectively. Death and preservation in
ethanol may cause a small change in carbon isotope value in in-
vertebrate tissue. However, this change is not significant; therefore, this
method is acceptable to analyze the distinct isotope signatures of C3 and
C4 sources in arthropod tissue (Sticht et al., 2006).
2.5. Community data analysis
The number of captured individuals in pitfall traps does not directly
reflect the real taxa density but instead shows the current density, trap
susceptibility, and activity level (Southwood and Henderson, 2009);
therefore, we considered here the “activity-density” (hereafter referred
to as “activity”).
We used the rarefaction and extrapolation approach (Chao et al.,
2014; Colwell et al., 2012) to compare the epigeic arthropod diversity
between habitats. This approach uses a reference sample to estimate a
smooth species accumulation curve, thus allowing for comparisons
between communities while controlling for differences in both abun-
dance and sampling effort. We performed a sample-size based rarefac-
tion/extrapolation of arthropod diversity using summed activity data
from the five pitfall traps of each habitat plot based on Hill numbers
(qD, sensu Jost, 2006). qD is an ecologically intuitive measure for de-
scribing and comparing diversity (Jost, 2006). We considered the Hill
number of order 0 (0D, species richness) and 1 (1D, exponential of
Shannon′s entropy). 0D is not sensitive to species abundance and so
gives disproportionate weight to rare species. 1D weighs each species
according to its proportional abundance in the sample, and we can
interpret it as the number of common species in the community (Jost,
2006). We calculated 95 % confidence intervals (CI) for Hill numbers
by a bootstrap method to determine whether there were any significant
differences between habitats (when the 95 % CI did not overlap, this
indicates a significant difference).These analyses were run using the
iNEXT R package (Hsieh et al., 2016).
We performed permutational analysis of variance to detect between-
habitat differences in the activity of arthropods grouped in orders, fa-
milies, and subfamilies since many morphospecies presented low ac-
tivity. We performed this analysis by the "perm.anova" function of the
"RVAideMemoire" R package (Hervé, 2019) with 999 permutations and
included habitat as a fixed factor and the plot as a nested random factor.
We used a pairwise permutational t-test performed with the "pairwi-
se.perm.t.test" function of the "RVAideMemoire" R package to detect
where there were activity differences between the habitats (Hervé,
2019).
We compared the community structure of epigeic arthropods be-
tween habitats using Permutational Multivariate Analysis of Variance
(PERMANOVA) with two taxonomic resolutions, one containing only
the arthropod orders and another containing only the Araneae,
Coleoptera and Formicidae morphospecies. We performed the
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Pedobiologia - Journal of Soil Ecology 78 (2020) 150607
PERMANOVA with 999 interactions. Then, we used Analysis of
Similarity (ANOSIM) to make pairwise comparisons between habitats of
arthropod communities. In both analyses, we included the plot as a
strata argument. To visualize the observed pattern, we performed non-
metric multidimensional scaling (NMDS) ordinations. After, we applied
a similarity percentage analysis (SIMPER) to determine which orders,
and morphospecies contributed most to the within-group similarities
and dissimilarities between habitats (cut off: ∼70 % of the cumulative
contribution, Clarke, 1993). We showed just the top 10 morphospecies.
We applied permutation tests to find out the taxonomic groups for
which the differences between habitats is an important component of
their contribution to dissimilarities (999 permutations). Finally, we
used the indicator value (IndVal) index to identify habitat indicators at
order and morphospecies levels. This method combines measures of
specificity (relative abundance) and fidelity (frequency) to generate
indicator values, which are expressed as percentages. Higher IndVal
percentages reflect the high specificity and fidelity of a taxon (Dufrêne
and Legendre, 1997). We evaluated the statistical significance of the
IndVal using Monte Carlo random permutation tests. We considered as
habitat indicators those orders and morphospecies with indicator values
that were significant (p < 0.05) and greater than 50 %. We used the
Hellinger method in all analyses to lessen the effect of the most abun-
dant taxa (Borcard et al., 2011; Legendre and Gallagher, 2001). All
analyses were based on Bray–Curtis dissimilarity measure (except for
IndVal) and performed by functions in the “vegan” and “labdsv” R
packages (Oksanen et al., 2015; Roberts, 2016).
We fitted Generalized Linear Mixed-Effects Models (GLMMs) to test
if, in addition to habitat type, patch area also explains arthropod
richness, diversity, and activity. We fitted all models with Poisson error
distribution and the plot as a random effect to consider the nested
sampling design. We fitted the models with the "glmer" function of the
‘lme4′ package (Bates et al., 2018).
2.6. Stable isotope analysis
We used Stable Isotope Analyses in R program (SIAR) to estimate
the relative contribution of native C3 and C4 plants and exotic C4 grass
sources to epigeic arthropod diet. We did the analysis only with taxo-
nomic groups that we captured in both habitats (Table S2), referred to
below as shared taxa. SIAR is a Bayesian mixing model that explicitly
incorporates variability associated with consumers, food sources, and
trophic enrichment factors. This model uses Markov Chain Monte Carlo
simulations to determine probable contributions to the consumer diet of
the different food sources (Parnell et al., 2010), after specifying the
δ13C and δ15N of consumers and basal sources and the isotope fractio-
nation values (Δ) between them. We consider three basal sources: (i) C3-
plant leaf litter of woodland savanna shrub and arboreal species, (ii)
native grass litter of savannas (composed of C4 and C3 species), and (iii)
African grass litter of pastures (exotic C4 species). We obtained the δ13C
and δ15N values of these basal sources in previous studies in the same
habitats and from the literature (Bustamante et al., 2004; Miranda
et al., 1997; R. Pinheiro-Alves, unpublished data; N.L. Rodovalho, un-
published data). The mean values were -27.3 ± 1.7‰ (δ13C) and
0.9 ± 2.3‰ (δ15N) for C3 shrub and arboreal species, −16.5 ± 5.9‰
(δ13C) and −1.7 ± 0.7‰ (δ15N) for native grasses, and
−13.0 ± 1.0‰ (δ13C) and 0.7 ± 2.7‰ (δ15N) for exotic grasses. We
assumed the Δ13C and Δ15N values to be +0.5 ± 1.2‰ and
+2.3 ± 0.2‰, respectively, as reported by McCutchan et al. (2003).
We used the simmr package in R to solve mixing model equations to
infer the probabilistic proportions of the native and exotic sources
consumed by each taxonomic group isotopically analyzed. The isotopic
mixing model is also based on a Bayesian framework and was run via
the ‘simmr_mcmc’ function (Markov chain Monte Carlo—MCMC) to
produce 1000 iterations over four MCMC chains (Parnell, 2016). Here
we also used the δ13C and δ15N values of the three basal sources used in
the SIAR analysis. We only presented the comparisons between
V.T. Pompermaier, et al. Pedobiologia - Journal of Soil Ecology 78 (2020) 150607

Table 1
The relative contribution of epigeic arthropod activity-density and permutational ANOVA results of activity-density comparisons between woodland savanna (Sav),
savanna-pasture boundary (Bou), and exotic pasture (Pas) habitats. The table shows the relative contribution of each order concerning total epigeic arthropod
activity-density (Order) and the relative contribution of each taxon concerning their higher taxonomic level (Taxa). The permutational ANOVA results are presented
by the F values with asterisks indicating where the permutation test found significant differences in mean taxa activities between habitats. The pairwise permutation
t-test show where the taxa activity-density significantly differ between habitats.
TAXON ORDER (%) TAXA (%) PERMUTATIONAL ANOVA PAIRWISE PERMUTATIONt testS

Class/Order Family/Subfamily Sav Bou Pas Sav Bou Pas F(2,30) Sav x Bou x Pas

ARACHNIDA
Acari 79.97 86.87 89.21 0.010
Opilioacarida 0.07 0.11 0 1.03 1.53 0 2.065
Oribatida 1.25 2.45 2.22 18.18 34.80 41.45 3.303
Galumnidae 37.74 45.85 62.08 8.632* Sav < Bou | Sav < Pas | Bou = Pas
Unidentified 62.26 54.15 37.92 0.634
Trombidiformes 2.00 0.96 1.42 29.16 13.58 26.42
Anystidae 34.12 33.75 2.61 4.732* Sav = Bou | Sav > Pas | Bou > Pas
Bdellidae 6.47 15.00 4.58 0.583
Cunaxidae 4.71 18.75 13.07 1.159
Erythraeoidea adults 31.76 22.50 13.07 3.281
Erythraeoidea larvae 22.94 10.00 66.67 5.349* Sav > Bou | Sav = Pas | Bou < Pas
Acari (Unidentified) 3.55 3.53 1.72 51.63 50.08 32.12 1.918
Araneae 1.63 1.04 0.65 18.93 12.83 10.79 12.703** Sav > Bou | Sav > Pas | Bou = Pas
Actinopodidae 1.45 1.15 0 1.714
Anapidae 0.72 0 0 1.000
Barychelidae 0.72 0 0 1.000
Caponidae 0 5.75 0 3.330 Sav < Bou | Sav = Pas | Bou > Pas
Clubionidae 0 1.15 0 1.000
Corinnidae 7.25 12.64 27.14 1.345
Ctenidae 6.52 2.30 1.43 0.444
Dipluridae 0 0 1.43 1.000
Gnaphosidae 3.62 6.90 4.29 0.528
Hahniidae 0.72 1.15 0 0.440
Lycosidae 10.14 22.99 20.00 0.705
Miturgidae 0 2.30 2.86 1.454
Oonopidae 2.90 1.15 1.43 1.384
Oxyopidae 1.45 1.15 4.29 0.545
Prodidomidae 0 1.15 0 1.000
Salticidae 2.17 4.60 2.86 0.442
Scytodidae 0.72 0 1.43 0.431
Tomisidae 0 0 1.43 1.000
Zodariidae 44.93 8.05 1.43 19.131*** Sav > Bou | Sav > Pas | Bou = Pas
Zoridae 5.80 2.30 0 5.473* Sav = Bou | Sav > Pas | Bou = Pas
Unidentified 16.67 37.93 30.00 0.108
Opiliones 0 0.02 0.04 0 0.29 0.62 1.714
Pseudoescorpiones 0.06 0.01 0 0.69 0.15 0 9.333** Sav > Bou | Sav > Pas | Bou > Pas
Scorpiones 0.04 0.01 0 0.41 0.15 0 3.500* Sav > Bou | Sav > Pas | Bou > Pas
CHILOPODA
Geophilomorpha 0.06 0.01 0 100 12.50 0 6.000* Sav > Bou | Sav > Pas | Bou > Pas
Scutigeromorpha 0 0.08 0.12 0 87.50 100 1.326
DIPLOPODA
Polydesmida 0 0 0.01 0 0 7.69 1.000
Polyxenida 0.02 0.26 0.07 33.33 95.65 61.54 1.932
Spirobolida 0.05 0.01 0.04 66.67 4.35 30.77 0.642
COLLEMBOLA
Entomobryomorpha 14.16 19.05 15.78 48.16 40.77 27.08 0.874
Symphypleona 9.61 21.26 26.53 32.68 45.50 45.52 9.896** Sav < Bou | Sav < Pas | Bou = Pas
Poduromorpha 5.63 6.42 15.97 19.17 13.73 27.40 5.679* Sav = Bou | Sav < Pas | Bou < Pas
INSECTA
Blattodea 0.45 0.51 0.01 0.72 1.15 0.03 10.871** Sav = Bou | Sav > Pas | Bou > Pas
Coleoptera 14.89 10.18 4.04 24.08 22.77 11.43 9.137** Sav = Bou | Sav > Pas | Bou > Pas
Bostrichidae 0.08 0.12 0.23 0.000
Carabidae 0.32 0.94 0.23 6.434* Sav = Bou | Sav = Pas | Bou > Pas
Chrysomelidae 0.16 0.12 0.92 1.217
Corylophidae 3.48 6.81 10.76 0.468
Curculionidae 0.63 1.17 0.46 3.924
Platypodinae 0.32 0.47 0.23 1.000
Scolytinae 2.93 4.11 5.03 0.807
Nitidulidae 40.62 31.81 23.34 8.322** Sav = Bou | Sav > Pas | Bou > Pas
Ptiliidae 14.25 7.28 0 5.658* Sav = Bou | Sav > Pas | Bou > Pas
Scarabaeidae 1.35 2.46 3.89 0.168
Silvanidae 0.08 0.35 1.60 3.500
Staphylinidae 28.90 34.51 30.21 7.004** Sav = Bou | Sav > Pas | Bou > Pas
Pselaphinae 0.32 0.12 0.23 1.161
Tenebrionidae 0.24 0.82 4.58 6.405* Sav = Bou | Sav < Pas | Bou < Pas
Unidentified 6.33 8.92 18.31 0.008
Dermaptera 0.04 0.12 0.01 0.06 0.27 0.03 3.941* Sav < Bou | Sav = Pas | Bou > Pas
(continued on next page)

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V.T. Pompermaier, et al. Pedobiologia - Journal of Soil Ecology 78 (2020) 150607

Table 1 (continued)

TAXON ORDER (%) TAXA (%) PERMUTATIONAL ANOVA PAIRWISE PERMUTATIONt testS

Class/Order Family/Subfamily Sav Bou Pas Sav Bou Pas F(2,30) Sav x Bou x Pas

Heteroptera 0.50 0.39 0.07 0.80 0.88 0.21 9.573** Sav = Bou | Sav > Pas | Bou > Pas
Hymenoptera 28.83 29.97 28.75 46.63 67.04 81.32 0.779
Formicidae 93.09 92.46 95.01 0.829
Dolichoderinae 7.73 10.39 8.87 0.366
Dorylinae 5.18 1.47 0.14 1.760
Ectatomminae 0.97 0.99 1.05 1.258
Formicinae 11.46 10.82 3.42 2.798
Myrmicinae 71.72 74.17 85.07 1.283
Ponerinae 2.81 2.11 1.42 1.156
Pseudomyrmecinae 0.13 0.04 0.03 1.454
Platygastroidea 6.91 7.54 4.99 0.604
Isoptera 15.19 0.35 0.05 24.58 0.78 0.13 3.386* Sav > Bou | Sav > Pas | Bou > Pas
Nasutitermitinae 100 100 100
Mantodea 0.04 0.05 0.02 0.06 0.11 0.05 0.255
Orthoptera 0.91 1.41 0.93 1.47 3.15 2.64 1.719
Psocoptera 0.09 0.16 0.15 0.15 0.35 0.42 1.342
Sternorrhyncha 0.31 0.27 0.49 0.50 0.61 1.39 0.623
Thysanoptera 0.26 0.51 0.32 0.42 1.15 0.92 0.568
Insect larvae 0.33 0.78 0.51 0.53 1.74 1.44 1.290

* p < 0.05.
** p < 0.01.
*** p < 0.001. The signs indicate when a taxon has exhibited significantly higher (>) or lower (<) activity or when no activity differences (=) were found
between habitats.

resources that presented a probability greater than 50 %. analyses showed that the arthropod community structure by orders and
by morphospecies was weakly to strongly different between habitats,
respectively. The overall dissimilarity by orders ranging from 33 %
3. Results
(savanna versus boundary) to 36 % (boundary versus pasture) and 40 %
(savanna versus pasture). The overall dissimilarity by morphospecies
We counted 29,826 epigeic arthropods, distributed among five
ranging from 70 % (savanna versus boundary) to 79 % (boundary
classes (Insecta, Collembola, Arachnida, Diplopoda, and Chilopoda), 25
versus pasture) and 80 % (savanna versus pasture). Detailed informa-
orders, 38 families, 11 subfamilies and 344 morphospecies (95 spiders,
tion on the orders and top 10 morphospecies of epigeic arthropods that
138 beetles, and 111 ant morphospecies). Overall, Insecta (46.3 %) and
contributed the most to the observed difference (average dissimilarity
Collembola (46 %) classes comprised 92.3 % of the epigeic arthropods,
%) in the communities between habitats are shown in Table 2. We did
followed by Arachnida (7.4 %), Diplopoda (0.2 %), and Chilopoda (0.1
not detect habitat indicators at the order level by the IndVal analysis. At
%). We found more Insecta (62 %) than other classes of epigeic ar-
the morphospecies level, the IndVal revealed only Staphylinidae (In-
thropods in the savannas, more Collembola (58 %) in the pastures, and
dVal = 57 %), Ptiliidae (IndVal = 55 %) and Zodariidae (IndVal = 54
similar proportions of Collembola (47 %) and Insecta (45 %) in the
%) morphospecies as savanna indicators.
boundaries. The Arachnida class comprised 9 %, 8 % and 6 % of the
Habitat type was identified by GLMM models as the main ex-
total epigeic arthropods in the savannas, boundaries, and pastures, re-
planatory factor for the significant changes of epigeic arthropod rich-
spectively. The proportions of all taxa are presented in Table 1.
ness, diversity, and activity between savanna and pasture (Table 3).

3.1. Epigeic arthropod community

We observed a lower richness (0D) and diversity (1D) of epigeic
arthropods in the pastures compared to the savanna and boundary
habitats, which did not differ (Fig. 1).
The permutational analyses of variance revealed that activity for
several predator groups significantly declined in pastures, such as
Anystidae mites, spiders, pseudoscorpions, scorpions and
Geophilomorpha centipedes, but also cockroaches, beetles, and termites
(Table 1). Significant activity increases in pasture mainly from meso-
fauna groups such as Symphypleona and Poduromorpha springtails and
Galumnidae mites was also observed (Table 1).
The PERMANOVA detected significant differences in the epigeic
arthropod community structure both by orders (F2,42 = 2.767;
p < 0.05) and morphospecies (F2,42 = 3.549; p < 0.05) resolutions.
The ANOSIM detected differences in order resolution only in savanna
versus pasture comparison (Global test, R = 0.22, p < 0.05). In mor-
phospecies resolution, ANOSIM revealed differences between all pair-
wise comparisons: savanna versus boundary (Global test, R = 0.20,
p < 0.05); savanna versus pasture (Global test, R = 0.45, p < 0.05);
boundary versus pasture (Global test, R = 0.25, p < 0.05). These
patterns can be seen in the NMDS ordinations (Fig. 2). The SIMPER
3.2. Diet modeling
All SIAR models showed high uncertainties in the 95 % credibility
intervals (Fig. 3). The SIAR model with shared taxa indicated that
epigeic arthropods feed mainly on C3 plant sources in the savanna, but
with signs of contribution coming from C4 exotic grasses even greater
than native ones (Fig. 3). Boundary arthropods presented a more ba-
lanced consumption of the three sources (Fig. 3). The native and exotic
grasses were the predominant food source of the pasture arthropod diet,
but with isotopic signals also indicating the contribution of C3 plants
(Fig. 3).
Two morphospecies of Scarabaeidae and one of Staphylinidae con-
sumed a greater amount of native grass sources in the savanna (more
than 50 % probability). With lower probability, the remaining analyzed
groups feed mostly on C3 native plants and grasses (Table S2). Araneae,
Dermaptera, and some Coleoptera and Myrmicinae morphospecies
consumed more native sources at the boundary (more than 50 %
probability), but a higher number of groups consumed more exotic C4
grasses compared to savanna (Table S2). At the pasture, Araneae and
three ant morphospecies consumed more exotic C4 grass sources, and a
Staphylinidae morphospecies consumed more native ones (with more

5
V.T. Pompermaier, et al. Pedobiologia - Journal of Soil Ecology 78 (2020) 150607

Fig. 1. Sample-size-based rarefaction (solid lines) and extrapolation (dashed

lines, up to double the reference sample size) of arthropod diversity with
abundance data based on the Hill numbers 0D (species richness) and 1D (ex-
Fig. 2. NMDS plots of epigeic arthropod community structure in woodland
ponential of Shannon′s entropy) for the woodland savanna, savanna-pasture
savanna (black squares), savanna-pasture boundary (gray triangles) and exotic
boundary and exotic pasture habitats. The shaded regions represent the 95 %
pasture (light gray circles) habitats. Plots show NMDS ordinations of arthropod
confidence intervals, obtained by a bootstrap method.
orders (A) and Araneae, Coleoptera and Formicidae morphospecies (B). Ellipses
represent ordination confidence intervals (95 %).
than 50 % probability). With lower probability, the remaining groups
consumed more exotic sources (Table S2).
4.1. Impacts on the epigeic arthropod community

More than 30 years after conversion from woodland savanna ve-

4. Discussion
getation with approximately ten years of low-intensity management,
the pastures analyzed here were occupied by a less diverse epigeic ar-
Consistent with our hypothesis, the epigeic arthropod community in
thropod community, dominated by collembolans (mainly the order
exotic pastures was significantly less rich and diverse and with a
Symphypleona) and Myrmicinae ants. Savanna-pasture boundaries
structure that differed from that of the woodland savannas. These re-
preserved the arthropod diversity of the savanna with a similar con-
sults are in line with the findings of similar studies in woodland savanna
tribution of beetles, but like pastures, showed a considerable proportion
vegetation (Benito et al., 2004; Luz et al., 2013; Marchão et al., 2009),
of collembolans. The initial changes that occur with the conversion of
and reinforce that continuous exotic pastures, even with small areas
savanna vegetation to pasture (e.g., slashing, burning, and transporting
and low management intensity, affect the soil fauna. Here we broaden
of surface soil) entirely or partially compromise the soil fauna, with
the knowledge about this impact to some mesofauna groups (discussed
recolonization only by groups accepting the new resources (Benito
below). The central novelty of this study was in quantifying the pro-
et al., 2004). The loss of epigeic arthropods richness and diversity in
portion of native and exotic plant sources consumed by the epigeic
these pastures is consistent with the global pattern of richness loss of
arthropods on savanna, boundary and pasture habitats. Despite the
arthropods and other animal groups in agricultural land types relative
uncertainty presented by the mixing models, they indicate that savanna
to native vegetation (Attwood et al., 2008; Newbold et al., 2015). Al-
arthropods can consume exotic sources and pasture arthropods can
though pastures can have lower impact on arthropods when they are
consume native ones. We discuss below this and other aspects of the
introduced into savanna-type vegetations (Decaëns et al., 2004) and
exotic pasture impact on epigeic soil fauna.
when compared to more intensive land use management (Attwood
et al., 2008), their use does not prevent the diversity loss of epigeic

6
V.T. Pompermaier, et al. Pedobiologia - Journal of Soil Ecology 78 (2020) 150607

Table 2 Table 3
Results of the similarity percentage (SIMPER) analysis of pairwise habitat Generalized Linear Mixed-Effects Models (GLMMs) fitted with the epigeic ar-
comparisons. The table shows the orders and top 10 morphospecies contribu- thropod richness, true diversity, and activity-density as a function of habitat
tion (%) to the average between-habitats dissimilarity. Average abundance was type (woodland savanna and exotic pasture) and patch area. Models were fitted
standardized by the Hellinger method. Asterisks indicate the groups detected by with Poisson error distribution and with the pitfall point coordinates as a
permutation tests for which the differences between habitats is an important random effect.
component of their contribution to dissimilarities.
Estimate SE z value
Taxa Average abundance Average dissimilarity %
Poisson model for richness
Savanna Boundary Intercept 3.953 0.043 91.361***
Habitat type −0.268 0.073 −3.677**
Orders Patch area 0.007 0.035 0.205
Symphypleona 0.25 0.32 4.65 Poisson model for true diversity
Poduromorpha 0.16 0.20 3.43 Intercept 2.857 0.095 29.983***
Isoptera 0.16 0.04 3.12** Habitat type −0.802 0.166 −4.826***
Hymenoptera 0.56 0.58 2.97 Patch area −0.095 0.079 −1.200
Entomobryomorpha 0.36 0.36 2.86 Poisson model for activity-density
Coleoptera 0.39 0.35 2.53 Intercept 6.058 0.141 42.941***
Trombidiformes 0.15 0.10 1.63 Habitat type 0.566 0.228 2.480*
Oribatida 0.11 0.15 1.58 Patch area 0.226 0.116 1.953
Morphospecies
Myrmicinae sp1 0.25 0.35 2.26 * p < 0.05.
Myrmicinae sp3 0.18 0.13 2.25 ** p < 0.01.
Nitidulidae sp2 0.34 0.22 2.05 *** p < 0.001. SE = Standard error.
Crematogaster sp1 0.15 0.01 1.75**
Ptiliidae sp1 0.18 0.10 1.59
Myrmicinae sp6 0.01 0.14 1.50 resource availability, nutrient cycling, and soil attributes (Barros et al.,
Dolichoderinae sp1 0.21 0.21 1.38 2004; Benton et al., 2003).
Myrmicinae sp18 0.01 0.12 1.37 Agricultural land uses can negatively affect arthropod abundance,
Staphylinidae sp1 0.22 0.22 1.31 mainly of predators and decomposer groups (Attwood et al., 2008).
Formicinae sp2 0.11 0.01 1.17**
Orders
This pattern was seen here by the activity decline of some predators,
Symphypleona 0.32 0.38 6.14* but not for decomposer groups such as Symphypleona and Podur-
Poduromorpha 0.20 0.35 5.81* omorpha springtails for which higher activity was found in the pas-
Hymenoptera 0.58 0.53 3.95 tures. The reduction of predators in pastures established in the wood-
Entomobryomorpha 0.36 0.28 3.06
land savannas has previously been reported (Benito et al., 2004; Franco
Coleoptera 0.35 0.23 2.83
Trombidiformes 0.10 0.10 1.96 et al., 2016), reinforcing that predators depend on more complex ha-
Orthoptera 0.13 0.11 1.56* bitats. Evidence suggests that a complex habitat shelters more natural
Morphospecies enemies (predators and parasitoids), possibly because they have more
Myrmicinae sp1 0.35 0.22 3.81** abundant prey, provide refuge against predation (cannibalism and in-
Myrmicinae sp3 0.13 0.21 3.02
traguild predation), improve prey capture efficiency, and provide a
Staphylinidae sp1 0.22 0.07 2.34***
Dolichoderinae sp1 0.21 0.05 2.20*** more favorable microclimate (Langellotto and Denno, 2004). Another
Myrmicinae sp12 0.03 0.15 1.87* critical aspect to consider regarding the introduction of pastures in
Myrmicinae sp6 0.14 0.16 1.83* tropical ecosystems is reduction of plant diversity, which can affect
Myrmicinae sp18 0.12 0.06 1.72
groups with more specific feeding habits (e.g., xylophagous termites)
Nitidulidae sp2 0.22 0.17 1.68
Myrmicinae sp4 0.00 0.12 1.61 and favor others such as grass-feeder termites (Carrijo et al., 2009;
Myrmicinae sp10 0.10 0.08 1.36 Oliveira et al., 2013). The activity decline of Nasutitermitinae termites
Orders in the present study pastures may indicate this aspect, but due to the
Poduromorpha 0.16 0.35 5.99** sampling method, we cannot observe the significant increase of some
Symphypleona 0.25 0.38 5.82
termite species already found in pastures introduced in the woodland
Hymenoptera 0.56 0.53 3.93
Coleoptera 0.39 0.23 3.55*** savannas (Benito et al., 2004; Franco et al., 2016).
Entomobryomorpha 0.36 0.28 3.44 Significant structural changes in the epigeic arthropod community
Isoptera 0.16 0.01 3.22** between savanna and pasture were confirmed for both orders (mainly
Trombidiformes 0.15 0.10 2.24*
of Collembola and Insecta) and Coleoptera and Formicidae morphos-
Morphospecies
Myrmicinae sp1 0.25 0.22 3.27
pecies. In the savanna versus boundary and boundary versus pasture
Myrmicinae sp3 0.18 0.21 2.95 pairwise comparisons, only Coleoptera and Formicidae morphospecies
Myrmicinae sp4 0.10 0.12 2.33 were important for the community structure dissimilarities between
Nitidulidae sp2 0.34 0.17 2.25** habitats. Factors behind these community changes are not yet fully
Ptiliidae sp1 0.18 0.00 2.13***
known in the woodland savannas but may be related to the quantity
Myrmicinae sp12 0.06 0.15 2.08
Staphylinidae sp1 0.22 0.07 2.06* and quality changes of available resources and pasture management.
Dolichoderinae sp1 0.21 0.05 2.06** Studies in temperate grasslands under acidic soils report micro-
Crematogaster sp1 0.15 0.00 1.91*** arthropod density increases concurrently with improvements in soil
Myrmicinae sp6 0.01 0.16 1.79
fertility and plant productivity (Cole et al., 2005), even with soil dis-
turbances due to trampling by grazing animals (Bardgett and Cook,
* p < 0.05.
** p < 0,01. 1998; Cole et al., 2008). Beetles were also among the groups markedly
*** p < 0.001. contributing to the structural community dissimilarity between savanna
and pasture, with Staphylinidae and Pitiliidae being important groups
arthropods as we found here. Although we have not tested this directly, for this habitat dissimilarity besides presenting high fidelity and spe-
it is possibly linked to habitat simplification (heterogeneity loss), mi- cificity to savannas. These groups can be quite sensitive to habitat
croclimate destabilization, decreased niche availability, and changes in changes and degradation due to their food habit specificity (Cristo

7
V.T. Pompermaier, et al.
Fig. 3. Relative contribution of C3-plants (woodland savanna shrub and ar-
boreal litter) native savanna grasses (C3 and C4 species) and exotic pasture
grass (C4 grass) sources for epigeic arthropod diet of woodland savannas (A),
savanna-pasture boundaries (B) and exotic pastures (C), performed by SIAR
models. Credible intervals of 1 %, 50 %, 75 %, and 95 % generated by a mixing
model are displayed from dark to light gray boxes.
8
Pedobiologia - Journal of Soil Ecology 78 (2020) 150607
et al., 2019), especially Ptiliidae beetles that are considered mycopha-
gous (Hammond and Lawrence, 1989) and usually found in decaying
organic debris, rotting trunks, and animal carcasses (Almeida et al.,
2015; Casari and Ide, 2012).
As with other animals, insects may also be affected by patch area
decrease (Hunter, 2002), but we need more experimental studies to
investigate this aspect in savanna vegetation. At least in a general way
we have seen that patch area did not affect the richness, diversity, and
activity of epigeic arthropods, making habitat type the main impact
factor for this community indicators. The functional consequences of
the exotic pasture impact to soil biota are still largely unknown in the
Brazilian savannas, but if it follows recent findings of multiple trophic
level studies, the biodiversity loss may be impairing the multi-
functionality of these ecosystems (Soliveres et al., 2016; Wagg et al.,
2014). Further studies on mechanisms behind exotic pasture impacts to
savanna epigeic arthropods are needed, concomitantly with the in-
vestigations of the soil fauna role to ecosystem multifunctionality. Here
we take the first step in better understanding the contribution of native
and exotic grasses to epigeic arthropod diet throughout savanna-pas-
ture habitats.
4.2. Arthropod consumption patterns of native and exotic sources
With few shared taxa and few sample replicates, our SIAR models
generated a great deal of uncertainty in the largest credible intervals.
Even so, our models suggest that woodland savanna arthropods are
more linked to native C3-plant sources, but have also grass sources
(mainly exotic) in their diet. The consumption of grass sources increases
at the boundary and is naturally higher in the pasture, but still with
signs of native C3-plant source consumption. These results possibly
demonstrate a cross-habitat spillover, i.e., the movement of organisms
across habitats (including foraging and dispersal events) that can shape
ecosystem processes and community composition in landscapes with
different habitat types (Tscharntke et al., 2012). No previous studies
have described cross-habitat spillover of insects in Brazilian savanna
landscapes, but our results indicate that stable isotope analyses can be a
useful tool for such investigations. However, we suggest that future
sampling designs consider increasing the exposure time of pitfall traps
to ensure that cross-habitat arthropods will be captured.
The three-source mixing model for all taxonomic groups analyzed
show that although most of the savanna taxa probably have native C3-
plant sources as their main diet, many probably consume more grass
sources. This association with grass sources may explain why the con-
version of vegetation types partially similar to pastures, such as sa-
vannas (due to grass layer presence), has less effect on soil macrofauna
than the conversion of forests for this purpose (Decaëns et al., 2004). In
the three-source mixing model, however, most of the taxa that consume
grass sources probably consume more native ones. So this dependence
on native sources may be a key factor explaining the decline of the
epigeic arthropod diversity and community structure change in the
pastures.
5. Conclusion
Exotic pastures are the primary land use in the Brazilian savanna
landscapes, which means that much of the local epigeic arthropod
biodiversity may already have been negatively affected, especially in
landscapes where few fragments of native savanna vegetation remain to
fulfill its conservation function. The distinct epigeic arthropod com-
munities found in pastures suggest that even low-intensity grazing
systems can impact arthropod groups that require more complex ha-
bitats (e.g., predators).
We report here that stable isotope analysis is a promising tool for
quantifying the proportion of native and exotic plant sources consumed
by savanna arthropods and detecting cross-habitat spillover events.
Pastures can maintain many arthropods already linked with a grass
V.T. Pompermaier, et al.
source diet, but only with the maintenance of savanna remnants in
agricultural landscapes will epigeic arthropods diversity be maintained
since some groups seem to be more dependent on native resources.
Future efforts to investigate the trophic niche of arthropods in different
land-uses and landscape configurations are needed to better understand
the cross-habitat spillover events and the importance of savanna frag-
ment conservation for the soil biodiversity and ecosystem functioning
maintenance in the Brazilian savanna.
Declaration of Competing Interest
All authors declare that the manuscript has not been considered for
publication elsewhere, and contributed to the writing and approved the
submitted version to Pedobiologia, and have no conflicts of interest.
Acknowledgments
We thank the Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq) for the scholarship granted to the first author and
for the financial support (Process: 454969 / 2014-7) to carry out this
work. We are grateful to Ray Pinheiro Alves for his support and pro-
viding data. We thank Vinicius Dufau for his help in identifying spiders.
We also thank Kathleen LaPoint, MS, ELS (board-certified Editor in the
Life Sciences) for providing editorial support and Jim Hesson for
proofreading the final manuscript.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.pedobi.2019.150607.
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