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MYRMECOFAUNA (HYMENOPTERA: FORMICIDAE) AS A BIOINDICATOR OF THE

QUALITY OF SOILS SUBMITTED TO THE APPLICATION OF PIG FARMING WASTEWATER

Myrmecofauna (Hymenoptera: Formicidae) como bioindicador da qualidade dos solos submetidos à aplicação da água
residuária da suinocultura

Dinéia Tessaro1*; Silvio Cesar Sampaio2; Elisandra Pocojeski3

1Professor;Doutor em Engenharia Agrícola; Universidade Tecnológica Federal do Paraná – Campus Dois Vizinhos; e-mail:
[email protected]
*Autor para correspondência
2Professor; Doutor em Engenharia Agrícola; Universidade Estadual do Oeste do Paraná – Campus Cascavel; e-mail:

[email protected]
3Professor; Doutor em Ciência do Solo; Universidade Tecnológica Federal do Paraná – Campus Dois Vizinhos; e-mail:

[email protected]

Artigo enviado em 30/06/2017, aceito em 24/11/2017 e publicado em 20/12/2017.

Abstract - The structure of ant communities is of particular interest as a bioindicator, given their importance in
environmental impact studies, as they present abundance and species richness, specialized taxa, wide geographical
distribution, and are easily sampled, in addition to being sensitive to environmental changes. Therefore, the objective
of this study was to evaluate the effects of wastewater application (0, 100, 200, and 300 m³ ha-¹) combined with
nitrogen fertilization (0 and 100% of the recommended dose for the crop) on the myrmecofauna in plantations of
minimilho in the municipality of Cascavel, PR. To evaluate the myrmecofauna, pitfall traps were installed and
organisms were classified by gender. The Formicidae family exhibited increased density up to 200 m 3 ha-1 doses of
pig farming wastewater, but no changes were observed in response to chemical fertilization. However, when sorted
by gender at the taxonomic level, no significant effects were observed on the different groups, except for the
Solenopsis genus following the use of 0 or 300 m3 ha-1 pig farming wastewater.

Keywords - edaphic fauna, edaphic ants, water reuse in agriculture.

Resumo - A estrutura das comunidades de formigas é de particular interesse como bioindicadoras dada sua
importância em estudos de impacto ambiental, uma vez que apresentam abundância e riqueza de espécies, táxons
especializados, ampla distribuição geográfica, facilmente amostrada, além de serem sensíveis às mudanças ambientais.
Considerando o exposto O objetivo do trabalho foi avaliar os efeitos da aplicação de água residuária da suinocultura
(0, 100, 200 e 330 m³ ha-¹) combinada com adubação nitrogenada (0 e 100% da dose recomendada para a cultura)
sobre a mirmecofauna em plantações de minimilho no município de Cascavel – PR.”. Para a avaliação da
mirmecofauna, foram instaladas armadilhas de queda sendo os organismos classificados ao nível de gênero. A família
Formicidae teve densidade aumentada até a dose 200 m3 ha-1 de água residuária da suinocultura, contudo sem
mostrar alterações decorrentes da adubação química. No entanto, a classificação ao nível taxonômico de gênero
demonstrou não existir efeitos significativos sobre os diferentes grupos, exceto para o gênero Solenopsis, quando
utilizadas as doses de 0 e 300 m3 ha-1 de água residuária da suinocultura.

Palavras-chave - fauna edáfica, formigas edáficas, reuso de água na agricultura.

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INTRODUCTION et al,. 2010); in the rehabilitation of mined areas and

degraded areas (ROSADO et al., 2014, RIBAS et al.,
Brazil displays indicators in pig farming of 2012b, ROCHA et al., 2015); in revegetation of riparian
high productivity in advanced technology, and is areas (GOLLAN et al., 2011); and in forest
positioned among the top countries for increasing pig disturbances (LEAL et al,. 2012; MIRANDA et al.,
production. This is because Brazil possesses state-of- 2013). Such potential is due to the high abundance and
the-art technology in all areas of pig production: species richness of these specialized groups, their wide
genetics, nutrition, sanitation, management, facilities, geographical distribution, sampling facilities, and their
and equipment. (ABCS, 2011; 2016). However, high sensitivity to changes in environmental conditions
production per unit area leads to the accumulation of (HOFFMANN and ANDERSEN, 2003). Ants are
effluents in the properties, which in most cases, exceed distributed in 327 genera and 16 subfamilies, and
the agricultural area required to absorb the production 13,188 species exist (BOLTON, 2016). Of these, 119
waste (SEGANFREDO, SOARES and KLEIN, 2003). genera are found in the Neotropical region, belonging
Under this scenario, environmental agencies have to eight subfamilies, with about 3,100 described species
shown great concern, since when the soil bearing (FERNÁNDEZ and OSPINA, 2003).
capacity is exhausted, this waste can cause a large Based on the above, coupled with the lack of
amount of environmental damage (Seidel et al., 2010). information on ants in relation to organic fertilization,
In this regard, studies investigating water reuse in the this study aimed to evaluate the effect of pig farming
environment have gained importance, and are usually wastewater (PFW) application combined with chemical
related to physical-chemical changes in the soil fertilization on the density and diversity of
(CAMPOS et al., 2012; LUCAS et al., 2013; myrmecofauna in typic dystroferric Red Latosol
MENEGHETTI et al., 2013; KESSLER et al., 2013; cultivated with baby corn in a subtropical region.
KESSLER et al., 2014; MAFRA et al., 2014),
contamination of surface and groundwater (MAGGI et
al,. 2011; BOLZANI, OLIVEIRA and
LAUTENSCHLAGER 2012; MAGGI et al., 2013; MATERIAL AND METHODS
CAPOANE et al., 2015), and the contribution to crop
productivity (MENEGHETTI et al., 2012; CAMPOS This study was conducted in Cascavel, PR,
et al., 2013). Only recently have efforts been increased Brazil (24º 48 'S and 53 26' W), at an altitude of 760 m.
in studies on soil biology, especially those focused on The weather is humid subtropical (Cfa), with an
meso and macrofauna (ALVES et al., 2008; TESSARO average annual rainfall of 1,800 mm, hot summers,
et al., 2011; TESSARO et al, 2013; CASTALDELLI et infrequent frosts, and a tendency for rainfall to be
al., 2015: SILVA et al., 2016 ). concentrated in the summer months; however, there is
The addition of organic residues can influence no definite dry season. The average temperature is
soil biota, since they act as a food source and modify 20°C and average relative humidity is 75%. The soil of
soil temperature and coverage In addition, they contain the area studied is a typic dystroferric Red Latosol with
toxic substances and harmful heavy metals, which clayey texture (EMBRAPA, 2006), which, since 2006,
adversely affect the fauna (BARETTA et al., 2003; has received nutrients from the application of PFW
MELO 2006). In this regard, the need to identify and and nitrogen fertilization (NFR). Notably, the
quantify the disturbances caused by human activities in treatments used in this study have been consistent
diverse environments has attracted the attention of since 2006, ensuring a track record of 3 years of PFW
researchers searching for organisms that can monitor application combined with NFR for each treatment.
the degree of ecosystem integrity. Therefore, several At the beginning of the current study, the soil
studies have shown that ants have potential for use as was chemically characterized before treatments were
bioindicators of environmental quality, in natural or applied; the results are shown in Table 1.
altered areas (RIBAS et al., 2012a). Ants have been The PFW was collected in an integrated bio
studied in various types of environments and system composed of a bio digester followed by a
situations, such as areas subjected to burning sedimentation tank and stabilization pond., Chemical
(BOSCARDIN et al., 2014); contaminated areas characterization was performed according to the
(RIBAS et al., 2012c); agroforestry systems and agro- methodology of Apha et al. (1998) (Table 2).
ecosystems (GONZÁLEZ-VALDIVIA et al., 2013;
RAMÍREZ et al., 2012); crop-livestock systems
(CREPALDI et al., 2014); agricultural crops (COUTO

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Table 1. Chemical characterization of experimental parcels before application of wastewater and nitrogen fertilization
Treatment
Attribute NFR PFW
0 100 0 100 200 300
Sodium (mg dm-3) 2.91 2.50 2.66 2.50 3.00 2.66
Calcium (cmolc dm-3) 5.85 5.81 5.86 6.24 5.36 5.87
Magnesium (cmolc dm-3) 3.71 3.45 3.71 3.69 3.30 3.63
Potassium (cmolc dm-3) 0.35 0.45 0.22 0.30 0.49 0.59
H+Al (cmolc dm-3) 2.72 2.66 2.72 2.42 3.02 2.58
Sum of bases (cmolc dm-3) 9.93 9.72 9.82 10.24 9.16 10.10
CTC pH 7,0 (cmolc dm-3) 12.66 12.39 12.55 12.66 12.22 12.68
Organic Carbon (g dm-3) 12.67 11.50 11.80 12.04 12.11 12.39
Organic matter (g dm-3) 19.78 21.78 20.31 20.72 20.83 21.31
Sat. Bases (%) 72.06 77.88 77.32 80.64 74.36 67.56
Phosphorus (mg dm-3) 8.68 13.77 8.87 11.63 14.21 8.87
Iron (mg dm-3) 96.69 99.35 105.21 96.74 83.38 106.75
Manganese (mg dm-3) 62.16 62.52 60.47 63.91 61.07 63.91
Copper (mg dm-3) 10.72 10.49 10.39 10.31 10.80 10.93
Zinc (mg dm-3) 2.21 2.96 2.02 2.87 3.60 3.85
pH 6.48 6.55 6.55 6.61 6.36 6.55
Dry mass (kg h-1) 57.00 62.31 44.81 61.32 62.56 69.87
*PFW: pig farming wastewater (0, 100, 200, and 300 m3 in the baby corn crop cycle); NFR: nitrogen fertilization (0 - without addition of NFR;
100 - NFR dose recommended for the crop - 80 kg ha-1)

Table 2. Chemical characterization of pig farming wastewater.

Attribute Result
pH (CaCl2) 7.9
Electrical conductivity (dS m-1) 2.1
Turbidity (NTU) 278
DBO (mg L-1) 550
DQO (mg L-1) 1450
Total Nitrogen (mg L-1) 338.8
N-Nitrate (mg L-1) 0.40
N-Nitrite (mg L-1) 8.00
Total Phosphorus (mg L-1) 211.9
Potassium (mg L-1) 440.0
Sodium (mg L-1) 17.0
Calcium (mg L-1) 2.25
Iron (mg L-1) 75.0
Magnesium (mg L-1) 0.95
Manganese (mg L-1) 16.5
Copper (mg L-1) 12.5
Zinc (mg L-1) 76.5
Totals (mg L-1) 1481
Stationary Totals (mg L-1) 729.0
Volatile Totals (mg L-1) 671.0

PFW was applied in a single step, 7 days by direct seeding, providing a stand of 180,000 plants
before the sowing of baby corn, was sown on the ha-1. Given the needs of baby corn crop, which are
remains of oat culture. The variety BR 106, which has based on those of corn, NFR was applied at a dose of
an approximate cycle of 80 days, was sowed manually 80 kg ha-1 nitrogen in the form of urea. Fertilization

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was performed in two stages, by applying 30% of the population size, was estimated by converting the
recommended dose at sowing, and the remaining number of individuals per trap/day.
during the stage of development characterized by For each treatment, data were submitted to
three to four developed leaves. analysis of variance using the randomized blocks
The edaphic myrmecofauna was sampled experimental design, in a 2 × 4 factorial design (two
using pitfall traps installed in each experimental levels of fertilization, 0 and 80 kg/ha of N-urea, and
parcel; traps comprised flasks with a 6-cm diameter, four doses of PFW, 0, 100, 200, and 300 m3 ha-1) for
buried in the ground, with the hollow end level with a total of eight treatments performed in triplicate.
the soil surface Preservative solution (200 mL) of 4% When necessary, the mathematical model was
formaldehyde was placed in the traps. Samples were transformed (y = x0.5 + 0.5) to normalize the data,
collected at three different times: 7 days after sowing using the Open Source Software SISVAR, version 4.2
(DAS), at the 15th leaf stage (41 DAS), and after the (Ferreira 2003), adopting the F test at p < 0.05,
development of spikelets (72 DAS). In each followed by the Scott-Knott test at 5%.
collection, the traps remained in the field for 7 days
and their contents were identified in the laboratory to
the taxonomic level of genus, using a binocular RESULTS AND DISCUSSION
magnifying glass and dichotomous keys for Table 3 shows the results of the test
classification as detailed by Baccaro (2006) and comparing the mean ant density in the three study
Bolton (1994). Ant density, expressed as the periods.

Table 3. Average ant density of the Formicidae family (bodies/trap/day), collected on the, by treatment applied and
timepoint.

Treatment
NFR (%) PFW (m3 ha-1)
0 100 0 100 200 300
First collection – 7 DAS
3,54 A 4,13 A 4,16 A 3,21 A 5,26 A 2,97 A
Second collection – 41 DAS
3,86 A 3,19 A 2,54 A 2,80 A 6,14 B 2,61 A
Third collection – 72 DAS
3,22 A 2,26 A 1,69 A 2,57 A 4,35 B 2,35 A
*PFW: pig farming wastewater; NFR: nitrogen fertilization; DAS: days after sowing. Capital letters in the same row do not differ by the Scott-
Knott test at 5% probability.

The density of organisms belonging to the existence of specialized taxa that can perceive
Formicidae family was influenced by the use of environmental changes (SILVA and BRANDÃO
wastewater, and was highest with the 200 m3 ha-1 1999). The results (Table 3) show that initially (at 7
dose at 41 and 72 DAS compared with the other DAS), there were no differences between the doses
treatments. of PFW, probably because of the high mobility group
Ants are the dominant taxonomic group in and the similar quality of food between areas analyzed
most ecosystems, and are present in various habitats. without developed vegetation. According to Schmidt,
According to Marino et al. (2002) and Andersen et al. Ribas, Schoereder (2013), reduced vegetation cover
(2002), ants are regarded as a suitable bioindicator in can distinctly affect different myrmecofauna groups,
areas that have been subjected to human actions, with negative effects on specialist species in closed
such as soil management, industrial pollution, and the and cooler areas, and positive effects on specialized
successful rehabilitation of degraded areas, because of species in more open and warmer areas. Oliveira et al.
the strong association between the state of (2011), also described the important role of
vegetation, soil, and decomposition. Some group vegetation on these organisms, noting that increased
characteristics guarantee them, generally, this status, complexity of the vegetation contributes to greater
such as their high abundance, species richness, ease diversity and group density.
of sampling, separation into morpho-species, and the

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However, from the second collection, the conducted in other types of crops, such as those by
predilection of the group treated with 200 m3 ha-1 was Couto et al., (2010) in growing soybeans, Santos,
visible, with a gradual increase in density observed as Carrano-Moreira and Torres (2012) in sugarcane, and
the PFW dose increased up to 200 m3 ha-1. However, Costa, Campos and Margarido (2014) in the
a decrease in the density of the group was observed cultivation and management of green manure.
with 300 m3 ha-1, with levels very close to those It was also noted that in the three periods
reported with 0 m3 ha-1. evaluated, the Dolichoderinae subfamily, Dorymyrmex
The results also showed that over time (41 genus, were present at the highest density compared
DAS), there was a decrease in the density of these with the other subfamilies, although this tendency
organisms. This suggests that the systematic use of was not statistically significant. According to Macedo
PFW under the evaluated conditions can lead to (2004), this genus may occur in high abundance
reduced populations of local myrmecofauna. This because these ants reduce the number of native ants
result is consistent with the findings of Alves et al. close to their nests; they are very aggressive and can
(2008), whom, when using pig slurry stored in monopolize food sources, because of the strength of
dunghill for stabilization, observed that the the recruited workers. This aggressive behavior may
myrmecofauna behaved in the same way at similar result in the emergence of other, mainly
doses. Another factor that may have contributed to phytophagous insects, over the long term, since
this reduction in the present study was the long dry belonging to this genus can means the removal of
season (30 days), which coincided with the evaluation predatory species from the environment.
period up to 72 DAS. Among the species of ants found of the
Taken together, these results suggest that, Myrmicinae, the presence of the Acromyrmex genus
within certain limits (up to 200 m3 ha-1), the use of in the first sampling period was notable. This group is
effluents with the studied characteristics enhance soil characterized by species of leaf-cutting ants (Lacau et
conditions for myrmecofauna; however, it becomes a al., 2008), which are considered pests in agriculture, as
limiting factor at higher doses. they use fresh leaves, shoots, and flowers as
The response observed here is important, substrates for fungal cultivation (HÖLLDOBLER
because the structure of ant communities is critical in and WILSON 1990). Considering its negative
studies investigating environmental impacts, since potential relative to plant growth, the occurrence of
they maintain and restore soil quality, and act to this group is undesirable in agricultural systems.
redistribute particles, nutrients, and organic matter, Because of its occurrence during the first sampling
thus improving water infiltration into the soil, due to period, it is possible that this group was inhibited by
its increased porosity and aeration (LOBRY DE the application of nitrogen and PFW, making this a
BRUYN 1999). viable practice. However, further studies evaluating
There were no significant differences in this genus in response to these parameters are
NFR between the periods analyzed, suggesting that needed.
the use of nitrogen fertilizers in the doses applied The results of the first sampling did not reveal
here does not alter the population density of these any differences in the density of ants between genera
organisms. in any of the factors assessed. According to Wink et
Table 4 compares the mean ant density for al. (2005), this reflects the low quality of food in the
each subfamily and genus identified. soil and organic matter, because under this initial
In the three samples (Table 4), ants were condition, no differences in vegetation cover were
captured that belonged to five of the 14 subfamilies observed. However, small variations were observed
found in Brazil (Ponerinae, Formicinae, regarding the number of genera found under the
Dolichoderinae, Ecitoninae, and Myrmicinae) (Bolton different treatments. Of the 14 genera found at 7
2003), and to 16 distinct genera, with the highest DAS with the 0 NFR treatment, 12 were reported
number of collected genera from the subfamily with the 100% NFR dose (80 kg ha-1 of N-urea) and
Myrmicinae. The predominance of this subfamily with doses of 0 and 200 m3 ha-1, while 11 genera were
could be explained by their high natural abundance found with the 100 and 300 m3 ha-1 doses. However,
and for being a group of ants their remarkable these results do not necessarily indicate a preference
adaptability to many different ecological niches in the of the groups under different treatments, and may be
Neotropics (FOWLER et al., 1991). The dominance related to the high mobility of the groups moving
of this subfamily has also been reported in studies from one area to another (CORDEIRO et al., 2004).

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Table 4. Average density of edaphic ants in all genera (genus/trap/day) collected in pitfall traps following treatment
with different doses of PFW and NFR in the three samples.
Treatment
AND PFW
Subfamily Genus 0 100 0 100 200 300
First Collection – 7 DAS
Ponerinae Hypoponera 0.32 A 0.28 A 0.28 A 0.28 A 0.33 A 0.30 A
Pachycondyla 0.11 A 0.09 A 0.16 A 0.14 A 0.04 A 0.07 A
Formicinae Camponotus 0.13 A 0.09 A 0.21 A 0.02 A 0.16 A 0.04 A
Dolichoderinae Dorymyrmex 0.73 A 0.88 A 0.73 A 0.95 A 0.76 A 0.78 A
Tapinoma 0.11 A 0.14 A 0.00 A 0.02 A 0.42 A 0.07 A
Dolichoderus 0.21 A 0.36 A 0.33 A 0.02 A 0.57 A 0.23 A
Ecitoninae Nomamyrmex 0.20 A 0.67 A 0.38 A 0.09 A 1.14 A 0.14 A
Neivamyrmex 0.36 A 0.39 A 0.40 A 0.38 A 0.52 A 0.21 A
Myrmicinae Solenopsis 0.61 A 0.58 A 0.33 A 0.71 A 0.76 A 0.59 A
Pheidole 0.03 A 0.00 A 0.00 A 0.00 A 0.00 A 0.07 A
Atta 0.05 A 0.00 A 0.11 A 0.00 A 0.00 A 0.00 A
Olygomyermex 0.22 A 0.34 A 0.38 A 0,14 A 0.40 A 0.21 A
Acromyrmex 0.09 A 0.02 A 0.11 A 0.00 A 0.11 A 0.00 A
Cephalotes 0.03 A 0.08 A 0.07 A 0.09 A 0.07 A 0,00 A
Second Collection – 41 DAS
Ponerinae Hypoponera 0.29 A 0.35 A 0.54 A 0.35 A 0.21 A 0.19 A
Pachycondyla 0.10 A 0.15 A 0.14 A 0.14 A 0.07 A 0.16 A
Formicinae Camponotus 0.03 A 0.00 A 0.07 A 0.00 A 0.00 A 0.00 A
Brachymyrmex 0.01 A 0.01 A 0.00 A 0.00 A 0.00 A 0.04 A
Dolichoderinae Dorymyrmex 0.96 A 0.71 A 0.69 A 1.09 A 0.69 A 0.88 A
Tapinoma 0.16 A 0.08 A 0.07 A 0.26 A 0.09 A 0.07 A
Dolichoderus 0.05 A 0.05 A 0.07 A 0.14 A 0.00 A 0.02 A
Ecitoninae Nomamyrmex 0.13 A 0.03 A 0.02 A 0.04 A 0.26 A 0.00 A
Neivamyrmex 0.40 A 0.19 A 0.19 A 0.14 A 0.69 A 0.16 A
Eciton 0.02 A 0.05 A 0.02 A 0.00 A 0.11 A 0.02 A
Myrmicinae Solenopsis 0.63 A 0.70 A 0.49 B 0.28 A 0.54 A 1.33 B
Atta 0.19 A 0.14 A 0.04 A 0.16 A 0.21 A 0.23 A
Olygomyermex 0.72 A 0.71 A 0.09 A 0.11 A 2.40 A 0.26 A
Cephalotes 0.11 A 0.03 A 0.07 A 0.11 A 0.09 A 0.02 A
Third Collection – 72 DAS
Ponerinae Hypoponera 0.32 A 0.33 A 0.23 A 0.35 A 0.23 A 0.47 A
Pachycondyla 0.08 A 0.05 A 0.07 A 0.04 A 0.09 A 0.07 A
Formicinae Camponotus 0.00 A 0.03 A 0.00 A 0.07 A 0.00 A 0.00 A
Brachymyrmex 0.00 A 0.01 A 0.00 A 0.01 A 0.00 A 0.00 A
Dolichoderinae Dorymyrmex 0.74 A 0.78 A 0.64 A 1.40 A 0.33 A 0.69 A
Tapinoma 0.23 A 0.21 A 0.19 A 0.11 A 0.33 A 0.26 A
Dolichoderus 0.02 A 0.05 A 0.09 A 0.02 A 0.02 A 0.02 A
Ecitoninae Nomamyrmex 0.05 A 0.03 A 0.02 A 0.02 A 0.09 A 0.04 A
Neivamyrmex 0.19 A 0.19 A 0.19 A 0.07 A 0.30 A 0.19 A
Eciton 0.01 A 0.02 A 0.02 A 0.02 A 0.00 A 0.02 A
Myrmicinae Solenopsis 0.36 A 0.49 A 0.28 A 0.26 A 0.52 A 0.66 A
Pheidole 0.00 A 0.02 A 0.00 A 0.00 A 0.04 A 0.00 A
Atta 0.03 A 0.08 A 0.11 A 0.04 A 0.02 A 0.04 A
Olygomyermex 0.23 A 0.49 A 0.21 A 0.07 A 0.83 A 0.35 A
*PFW: pig farming wastewater; NFR: nitrogen fertilization; DAS; days after sowing. Capital letters in the same line do not differ by the Scott-
Knott test at 5% probability.

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The results presented in Table 4 indicate understand the interaction of these factors with the
there was no significant difference among ant genera studied group. In this case the importance of ants as
in response to NFR in all sampling periods, showing bioindicators is evident.
that the distribution of the groups was independent
of this factor.
Conversely, after 41 DAS, differences in the CONCLUSIONS
PFW factor were observed between doses of 0 and
300 m3 ha-1 in the Myrmicinae subfamily, Solenopsis The application of PFW induced significant
genus. The behavior of this genus differs in response positive effects on the Formicidae family up to a dose
to environmental quality. According to Fernandes of 200 m3 ha-1; however, no effect was found on the
(2003) and Nascimento, Morini, and Brandão (2001), density of organisms between the different genera.
this genus is common in disturbed areas, and adapts NFR did not affect the density of the
well to disturbed sites, justifying the increase in Formicidae family, or the studied genera.
response to PFW at 300 m3 ha-1 compared with the These results suggest that PFW can promote
other doses. However, in a study of the changes in the edaphic myrmecofauna; however,
myrmecofauna in a Pinus elliottii plantation, Matos et further studies of longer duration and with other
al. (1994) noted that high proportions of this group cultures should be performed to better understand
of ants occur in soils with low vegetation cover, the interaction of these factors with this group of
consistent with the result of the present study at 0 m 3 organisms.
ha-1, with reduced vegetation cover. This is reinforced
by the findings of Marinho et al. (2002), who
reported that this species was among the most REFERENCES
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