Center for Nuclear Energy in Agriculture, University of So Paulo, Av. Centenrio 303, 13416000, Piracicaba, SP, Brazil
Universidade Positivo, Rua Prof. Pedro de Souza 5300, 81280330, Curitiba, PR, Brazil
Santa Catarina State University, Rua Beloni Zanin 680E, 89815630, Chapec, SC, Brazil
d
Department of Soil Science, Luiz de Queiroz College of Agriculture, University of So Paulo, Av. Pdua Dias 11, 13418900, Piracicaba, SP, Brazil
e
School of Global Environmental Sustainability & Department of Biology, Colorado State University, 80523, Fort Collins, CO, USA
f
Shell Technology Centre Houston, 3333 Highway 6 South, Houston, TX 77082, USA
b
c
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
a r t i c l e
i n f o
Article history:
Received 17 November 2015
Received in revised form 5 April 2016
Accepted 17 April 2016
Available online 30 April 2016
Editor: D. Barcelo
Keywords:
Bioenergy crops
Land use change
Soil biodiversity
a b s t r a c t
Land use changes (LUC) from pasture to sugarcane (Saccharum spp.) crop are expected to add 6.4 Mha of new
sugarcane land by 2021 in the Brazilian Cerrado and Atlantic Forest biomes. We assessed the effects of these
LUC on the abundance and community structure of animals that inhabit soils belowground through a eld survey
using chronosequences of land uses comprising native vegetation, pasture, and sugarcane along a 1000-km-long
transect across these two major tropical biomes in Brazil. Macrofauna community composition differed among
land uses. While most groups were associated with samples taken in native vegetation, high abundance of
termites and earthworms appeared associated with pasture soils. Linear mixed effects analysis showed that
LUC affected total abundance (X2(1) = 6.79, p = 0.03) and taxa richness (X2(1) = 6.08, p = 0.04) of soil macrofauna. Abundance increased from 411 70 individuals m2 in native vegetation to 1111 202 individuals m2
in pasture, but decreased sharply to 106 24 individuals m2 in sugarcane soils. Diversity decreased 24% from
native vegetation to pasture, and 39% from pasture to sugarcane. Thus, a reduction of ~90% in soil macrofauna
abundance, besides a loss of ~ 40% in the diversity of macrofauna groups, can be expected when sugarcane
Corresponding author at: Department of Biology, Colorado State University, 80523, Fort Collins, CO, USA.
E-mail address: andre.franco@colostate.edu (A.L.C. Franco).
http://dx.doi.org/10.1016/j.scitotenv.2016.04.116
0048-9697/ 2016 Elsevier B.V. All rights reserved.
A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
161
crops replace pasture in Brazilian tropical soils. In general, higher abundances of major macrofauna groups (ants,
coleopterans, earthworms, and termites) were associated with higher acidity and low contents of macronutrients
and organic matter in soil. This study draws attention for a signicant biodiversity loss belowground due to tropical LUC in sugarcane expansion areas. Given that many groups of soil macrofauna are recognized as key mediators of ecosystem processes such as soil aggregation, nutrients cycling and soil carbon storage, our results warrant
further efforts to understand the impacts of altering belowground biodiversity and composition on soil functioning and agriculture performance across LUC in the tropics.
2016 Elsevier B.V. All rights reserved.
1. Introduction
One of the central sustainability issues related to the rapid growth of
bioenergy industry refers to the implications of large-scale biofuel feedstock cultivation on biodiversity (Dauber and Bolte, 2014; Wiens et al.,
2011). Land use changes (LUC) associated with bioenergy feedstock
production appear as a key driver of above and belowground biodiversity changes due to the demand for biofuels, and the negative impacts
are primarily reported from tropical regions (Desiree et al., 2014;
McCormack et al., 2013). In Brazil, sugarcane (Saccharum spp.) is the
single plant used for ethanol fuel production and the additional amount
of land under sugarcane necessary to meet the domestic demand for
ethanol for 2021 is projected to be 6.4 Mha (Goldemberg et al., 2014),
which is larger than the total area of countries such as Netherlands
or Switzerland. Typical LUC in Brazilian sugarcane expansion areas
are the conversion of cultivated pastures into sugarcane elds
(Goldemberg et al., 2014). Roughly 70% of the new sugarcane elds
established between 2000 and 2010 in Brazil were previously cultivated
pastures used for cattle ranching (Adami et al., 2012). Those pastures
mostly replaced native vegetation areas between 1970 and 1980 by a
conversion that involves clearing native vegetation through traditional
slash and burn practices, and planting pasture grass in the same year.
Conversion of native vegetation directly into sugarcane have historically
accounted for less than 1% of the sugarcane expansion in Brazil (Adami
et al., 2012).
The existing literature does not show a clear position about the
effects of direct LUC for sugarcane expansion on biodiversity
(Goldemberg et al., 2008; Verdade et al., 2012). Particularly the responses of soil biodiversity to these LUC remain unexplored. Soil animals are estimated to represent as much as 23% of the total described
global diversity (Decaens et al., 2006). The larger soil invertebrates are
the soil macrofauna, with a body length longer than 2 mm (Swift
et al., 1979). Soil macrofauna are key mediators of ecosystem functions
for a variety of ecosystem engineering processes (Lavelle et al., 2006).
Soil macroinvertebrates actively inuence pedological processes
through structural and mineralogical transformations (de Oliveira
et al., 2014), and improve soil hydraulic properties such as aeration
and drainage (Leonard and Rajot, 2001). These animals also have an acknowledged role in building and stabilizing soil aggregates with direct
implications on ood and erosion control (Brussaard et al., 2007; Six
et al., 2004), soil carbon storage and net soil greenhouse-gas emissions
(Lubbers et al., 2013; Majeed et al., 2014). Moreover, these animals signicantly inuence nutrient cycling processes (de Vries et al., 2013;
Lubbers et al., 2013; Wagg et al., 2014).
We followed the progress of modications in soil macrofauna abundance and its community structure across LUC through a eld survey
using chronosequences of land use over two major tropical biomes in
Brazil. We predicted that sugarcane establishment over pasturelands
would reduce the soil macrofauna abundance as well as the diversity
of macrofauna groups. Rationale for this hypothesis is that the intensied land use in sugarcane crops compared to pastures would substantially reduce the quality and quantity of inputs available as well as the
soil micro-habitats, nally leading to loss of soil animals and simplication of the soil community, as it has been observed in other
agroecosystems (Callaham et al., 2006; Castellanos-Navarrete et al.,
2012; Hernandez-Ruiz and Castano-Meneses, 2006). Every ve years a
cultivation cycle is carried in sugarcane elds with plowing and fertilization for planting of new stem cuttings, reducing soil carbon stocks over
time (Franco et al., 2015; Mello et al., 2014) and potentially altering soil
structure and bulk density. Sugarcane farming is also characterized by
signicant inputs of persistent herbicides and controlled release pesticides (Bell et al., 2007). On the other hand, LUC from pasture to sugarcane promote signicant improvements on soil chemical quality by
increasing nutrient levels and reducing soil acidity due to inputs of fertilizers and lime (Cherubin et al., 2015), what gives rise to the hypothesis that detrimental LUC effects on soil macrofauna community would
be inversely related to soil chemical quality.
Our goal was to evaluate the effects of LUC to the expansion of
Brazilian sugarcane acreage on the soil macrofaunal community. Specifically, we wanted: (1) to compare soil macrofauna abundance, taxonomic richness, diversity and equability among different land uses;
(2) to investigate the vertical distribution of soil macrofauna abundance
and richness within the soil pedon as a function of LUC; (3) to explore
the relationships between macrofauna biodiversity and soil chemical attributes (soil acidity, and contents of soil organic carbon (SOC) and
macronutrients).
2. Materials and methods
2.1. Description of the study sites
The study was carried out in the main sugarcane production region
in the world, Central-Southern Brazil. Three study sites were identied
representing the Northern, Central, and Southern parts of the Brazilian
sugarcane growing region, including the areas where sugarcane expansion is occurring from pastures: Northern, Lat_17S, located in the city of
Jata, Southwestern region of Gois state (175616S, 513831W);
Central, Lat_21S, located in the city of Valparaso, West region of So
Paulo state (211448S, 504704W); and Southern, Lat_23S, located
in the city of Ipaussu, South region of So Paulo state (230508S,
493752W) (Fig. 1).
In each study site we identied a chronosequence of land use for: native vegetation, pasture, and sugarcane crop, and to minimize the effects
of climatic, topographic and edaphic variations, the three land uses were
always located in adjacent areas within sites. Climate and soil characteristics can be found in Table 1. A complete soil chemical characterization
can be found in Cherubin et al. (2015), and detailed information on the
past history of land use and soil management in the study sites is provided in Table A.1. Briey, native vegetation at Lat_17S comprises the
Cerrado forest formation, while at Lat_21S and Lat_23S it comprises a
transition between the Atlantic forest and Cerrado vegetation. LUC
from native vegetation to pasture happened in 1980 at both Lat_17S
and Lat_21S, and in 1979 at Lat_23S. Pasture areas differed from each
other in the stocking rate: 1.5 animal unit (AU, or a 454 kg cow with
or without an unweaned calf) ha1 at Lat_17S; around 2 AU ha1 at
Lat_21S; and around 1 AU ha1 at Lat_23S along the year. Sugarcane
was established over part of the pasture area in 2009 at Lat_17S, in
2010 at Lat_21S, and in 1990 at Lat_23S. The nutrient inputs in sugarcane differed among the sites, with annual inputs of mineral P at
Lat_17S and Lat_21S, and high amounts of organic fertilizers at
Lat_23S. The temporal differences in LUC time added to the contrastive
soil types among sites enlarged the strength of the data set taken.
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2.2. Sampling
The eld sampling for soil macrofauna was carried out in the rainy
season, in January 2013. High soil fauna richness and reduced variation
of abundance are expected during the rainy season, which is therefore
more indicated for the assessment of soil fauna (Neto et al., 2012). All
samples from a single site were taken on the same day. At each site macrofauna samples were extracted from a 1-ha grid with 9 sampling points
spaced 50 m apart. Soil blocks of 25 25 cm to 10 cm depth were collected from 0 to 10 cm, 1020 cm, and 2030 cm soil layers at each sampling
point, and sorted according to the standard Tropical Soil Biology and Fertility Institute (TSBF) soil monolith method (Anderson and Ingram, 1993;
Moreira et al., 2008). In total 81 monoliths were excavated. The animals
were carefully hand-sorted from the soil blocks in a large tray, immediately after the sampling procedure. Operationally macrofauna have been dened here as the groups in which its individuals are visible to the naked
eye (Kevan, 1968). Organisms from the litter were added with the
010 cm soil macrofauna. The earthworms were preserved in 92.8% ethanol and all the others individuals in 70% ethanol for subsequent laboratory identication and counting. The invertebrates were sorted into the
taxonomic groups: Aranae, Blattodea, Chilopoda, Coleoptera, Dermaptera,
Diplopoda, Diptera, Formicidae, others Hymenoptera, Gastropoda,
Hemiptera, Isopoda, Isoptera, Oligochaeta, and Scorpiones.
Samples for soil chemical characterization were taken at the same
points and time of the macrofauna data, and these data were used to
verify correlations between soil chemical attributes and soil macrofauna. Within a radius of 6 m around each central monolith used
for macrofauna extraction, 12 subsamples were collected from 0 to
10 cm, 1020 cm, and 2030 cm soil layers using a soil Dutch
auger, and composited for subsequent analyses. Soil chemical attributes were measured by analytical methods described in van Raij
et al. (2001): active acidity (pHCaCl2 0.01 mol L 1), potential acidity
(H + Al) by SMP solution, available calcium (Ca) and magnesium
(Mg) by ion-exchange resin/atomic absorption, potassium (K) by
ion-exchange resin/atomic emission, phosphorus (P) by ionexchange resin/colorimetry, and sulfur (Ssulphate) by calcium
phosphate/turbidimetry. SOC and nitrogen (N) were determined by
dry combustion on elemental analyzer LECO CN-2000 (furnace
at 1350 C in pure oxygen).
2.3. Data analysis
The faunal abundance was calculated as the number of individuals
per surface unit (m2). Faunal diversity was assessed by richness (number of groups), and the Shannon's diversity index (H), and evenness
(E). H is calculated by the formula:
H pi log2 pi:
i1
A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
163
Table 1
Climate, soil classication according to Soil Survey Staff (2014), and soil chemical characterization for the study sites.
Site
mm
(cm)
Lat_17S 1600
NV
PA
SC
Lat_21S 1240
NV
PA
SC
Lat_23S 1470
NV
PA
SC
a
b
c
Anionic Acrudox
010
1020
2030
Typic Hapludox
010
1020
2030
Anionic Acrudox
010
1020
2030
Typic Rhodudalf
010
1020
2030
Typic Kandiudult
010
1020
2030
Typic Hapludalf
010
1020
2030
Rhodic Hapludox 010
1020
2030
Rhodic Kandiudox 010
1020
2030
Rhodic Hapludox 010
1020
2030
Ca
Mg
SOCc
(mmolc dm3) (mmolc dm3) (mmolc dm3) (g kg1) (mmolc dm3) (mg dm3) (g kg1)
3.8
3.8
3.9
3.7
3.8
3.8
5.1
5.1
4.8
6.5
6.3
6.3
4.0
3.9
4.0
5.3
5.1
4.7
3.7
3.7
3.7
4.7
4.5
4.5
5.5
5.3
5.4
92.8
78.1
64.8
55.1
46.8
39.1
30.0
30.1
33.1
14.7
14.2
13.6
48.3
44.5
39.0
25.2
26.8
31.7
152.8
156.6
152.7
52.5
55.8
53.7
29.7
35.9
33.6
4.2
2.6
2.1
3.0
2.2
2.3
21.7
20.2
15.7
101.6
82.5
69.2
8.3
6.3
8.0
39.0
29.8
24.2
17.1
15.3
12.9
32.6
29.6
24.6
47.5
48.8
47.1
3.4
2.3
1.8
1.6
1.1
1.2
9.3
8.9
6.9
18.6
16.7
14.2
5.2
3.5
3.5
15.6
12.4
9.5
9.1
8.1
7.4
19.9
16.2
12.3
20.1
19.3
18.3
1.2
1.0
0.9
0.7
0.5
0.5
0.8
0.7
0.6
2.2
1.7
1.6
1.1
0.8
0.6
1.1
1.0
0.8
3.1
3.0
2.6
2.6
2.1
1.6
1.5
1.4
1.5
1.0
0.8
0.7
0.6
0.5
0.5
0.6
0.6
0.5
2.8
2.9
2.4
4.2
3.4
3.1
3.1
2.9
2.6
2.8
2.4
2.3
4.4
4.5
4.1
3.1
2.3
2.0
5.6
4.5
3.5
3.0
2.6
2.5
7.3
7.0
4.7
17.3
12.5
9.9
7.1
3.9
3.2
19.6
13.2
7.8
14.3
12.4
11.0
11.5
9.8
7.6
8.9
8.6
7.2
15.6
12.9
10.7
9.5
8.4
6.4
10.8
10.4
9.7
21.8
16.0
14.9
13.3
9.5
7.5
11.0
9.9
8.0
36.7
33.7
30.3
36.4
27.6
20.6
18.9
18.4
17.1
MAP = mean annual precipitation Obtained from CIIAGRO and CEPAGRI climate data from Jata, GO, Valparaso, SP, and Ipaussu, SP.
NV = native vegetation; PA = pasture; SC = sugarcane crop.
SOC = soil organic carbon.
H0
log2 s
E represents the distribution of taxa and assesses the balance of populations. E is equal to 1 when all taxa are of equal abundance and tends
to 0 when one or a few taxa largely dominate the community.
We performed a linear mixed effects analysis of the relationship between individual macrofauna variables (abundance, groups richness,
Shannon index, and evenness) and land use. As xed effects, we entered
land use and soil layer depth (without interaction term) into the model.
As random effects, we had intercepts for sites, as well as by-sites
random slopes for the effect of the macrofauna variable analyzed. Pvalues were obtained by likelihood ratio tests of the full model with
the effect in question against the model without the effect in question.
Macrofauna communities were ordinated with two methods: rst,
land uses were ordinated by their dissimilarity in groups composition
with non-metric multidimensional scaling (NMDS) on Bray-Curtis dissimilarity matrix of macrofauna groups abundance data to reduce dimensionality and allow the visualization of major patterns structuring
the community, followed by non-parametric multivariate analysis of
variance (npMANOVA) to test the effect of LUC and site; secondly, a
principal component analysis (PCA) was performed to visualize the correlations among the abundance of dominant macrofauna groups
(Isoptera, Oligochaeta, Coleoptera and Formicidae) and soil acidity, contents of SOC and contents of macronutrients. All analyses were conducted using the software R, version 3.2.2 (Team RDC, 2014), and we ran the
packages vegan (Dixon, 2003), lme4 (Bates et al., 2015), and ggplot2
(Wickham, 2009).
3. Results
Samples corresponding to native vegetation, pasture, and sugarcane
appeared separated on the NMDS plot (Fig. 2), suggesting that the abundance of the macrofauna groups varied among land uses. While most
groups were associated with samples taken in native vegetation, highly
abundant Isoptera and Oligochaeta appeared associated with pasture
soils (Fig. 2). Differences in community composition among land uses
were conrmed by npMANOVA (df = 2, F = 6.11, r2 = 0.12, p =
0.01) which also demonstrated a signicant effect of site (df = 1, F =
4.35, r2 = 0.04, p = 0.01), and land use site (df = 2, F = 2.91, r2 =
0.06, p = 0.01) on the abundances of the macrofauna groups.
Linear mixed effects analysis showed that land use affected total
abundance of macroinvertebrates (X2(1) = 6.79, p = 0.03), increasing
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A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
complete land use sequence (13% of the individuals under native vegetation, 17% under pasture, and 21% in sugarcane soils). Earthworms
accounted for 10% of the total individuals, and were proportionally
more abundant under anthropogenic land uses (17% of the individuals
under pasture and 12% of the individuals under sugarcane) than under
native vegetation (3%) (Table 2).
LUC did not affect Shannon index (H) (X2(1) = 3.55, p = 0.17)
(Fig. 3c). The overall H dropped from 1.6 0.2 in native vegetation to
1.0 0.2 in pasture, and to 0.7 0.2 in sugarcane soils. Although
there were no statistically signicant effects of LUC on evenness (E)
(X2(1) = 3.89, p = 0.14), there was a tendency for one or a few taxa
to dominate the community after LUC (Fig. 3d). The smallest value for
E (0.3 0.1) was found under pasture at Lat_17S.
The top layer 010 cm of the soil pedon harbored on average 69% of
the organisms. Under sugarcane an average of 87% of the organisms
were found in the 010 cm layer, while this value was 80% in native vegetation and 63% in pasture. Overall, macrofauna abundance decreased
by about 245.3 individual m2 59.74 from 0 to 10 to 1020 cm, and
by 275.3 59.74 from 0 to 10 to 2030 cm soil layer. Richness lowered
by about 1.68 groups 0.20 from 0 to 10 to 1020 cm soil layer, and by
1.95 groups 0.20 from 0 to 10 to 2030 cm soil layer. Despite substantially altering the abundance and taxonomic richness of the macrofauna
community, LUC did not change the vertical distribution based on the
proportion of taxa found in the different soil layers; there was a rate
of 2:1 between the number of taxa in the 010 cm layer and the number
of taxa in both 1020 cm and 2030 cm layers at all land uses (Fig. 4).
Fig. 5 shows the distribution of the sampling points colored according to the land use, with soil variables as explanatory variables. Together, the two axes explained 52.7% of the variance. In general, pasture soils
(green) were grouped near the macrofauna variables, while sugarcane
soils (blue) were mainly associated with higher pH and higher contents
of Ca and Mg. Native vegetation soils (red) were widely distributed.
Isoptera and Oligochaeta showed a weak negative correlation with pH.
The abundance of Isoptera, Oligochaeta and Coleoptera was negatively
Fig. 3. Soil macrofauna abundance (a), taxonomic richness (b), diversity (c), and taxa distribution (d) in the 030 cm soil layer as a function of the land use change. n = 9, error bars denote
standard error of the mean.
A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
165
Table 2
Abundance (individuals m2) and standard error of soil macrofuna groups in the 030 cm layer. n = 9.
Taxa
Common name
Taxonomic level
Lat_17S
Lat_21S
Lat_23S
NV
PA
SC
NV
PA
SC
NV
PA
SC
Earthworms
Oligochaeta
Earthworms
Subclass
4 (2.4)
9 (5.4)
4 (2.4)
21 (9.2)
373 (102.9)
25 (7.1)
9 (3.9)
60 (15.5)
11 (7.1)
Insects
Isoptera
Hymenoptera
Formicidae
Coleoptera
Blattodea
Dermaptera
Diptera
Hemiptera
Termites
Oth. than ants
Ants
Beetles
Cockroaches
Earwigs
Mosquitoes
Bugs
Order
Order
Family
Order
Order
Order
Order
Order
66 (26.7)
9 (3.9)
4 (2.4)
25 (10.7)
0
0
0
0
1093 (309.2)
0
55 (21.5)
308 (277.7)
0
0
0
0
0
4 (2.4)
0
11 (4.6)
0
2 (1.8)
0
0
11 (7.1)
7 (3.9)
144 (70.0)
82 (30.5)
0
11 (6.0)
12 (7.4)
2 (1.8)
78 (66.4)
2 (1.8)
78 (37.4)
247 (64.2)
0
16 (7.1)
0
0
0
2 (1.8)
2 (1.8)
21 (13.6)
0
2 (1.8)
0
0
151 (72.4)
0
272 (102.9)
25 (10.4)
2 (1.8)
0
5 (5.3)
0
924 (488.5)
0
14 (5.6)
5 (2.7)
0
0
0
0
2 (1.8)
0
55 (30.4)
20 (10.6)
0
0
0
0
Myriapods
Diplopoda
Chilopoda
Millipedes
Centipedes
Class
Class
4 (2.4)
2 (1.8)
0
7 (2.8)
14 (4.2)
0
44 (25.8)
16 (8.4)
0
9 (6.0)
92 (38)
36 (35.6)
32 (6.0)
82 (24.2)
30 (12.9)
5 (2.7)
7 (4.7)
9 (4.7)
Arachnids
Araneae
Scorpiones
Spiders
Scorpions
Order
Order
0
0
2 (1.8)
2 (1.8)
0
0
25 (7.6)
0
2 (1.8)
0
0
0
30 (11.8)
5 (5.3)
2 (1.8)
0
2 (1.8)
0
Molluscs
Gastropoda
Snails
Class
2 (1.8)
4 (2.4)
5 (3.8)
Crustaceans
Isopoda
Woodlouse
Order
37 (37.3)
84 (64.4)
9 (7.1)
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A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
Fig. 4. Vertical distribution and taxonomic group composition of soil macrofauna within soil pedon under native vegetation, pasture, and sugarcane at three eld sites. Numbers in italics
refer to total density in each layer. n = 9. Abbreviations: Aran = Aranae, Chi = Chilopoda, Col = Coleoptera, Dip = Diplopoda, Form = Formicidae, Isop = Isopoda, Isopt = Isoptera, and
Olig = Oligochaeta.
A.L.C. Franco et al. / Science of the Total Environment 563564 (2016) 160168
167
Fig. 5. Principal component analysis of the abundance of major macrofauna groups (Oligochaeta, Isoptera, Coleoptera, and Formicidae) and soil chemical attributes (pH CaCl2 (pH),
exchangeable aluminum (H + Al), calcium (Ca), magnesium (Mg), potassium (K), phosphorus (P), nitrogen (N), soil organic carbon (SOC), of 243 sampling points across three land
uses: native vegetation (red), pasture (green), and sugarcane (blue).
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