Sociobiology 61(3): 250-257 (September 2014) DOI: 10.13102/sociobiology.v61i3.

250-257

Sociobiology
An international journal on social insects

RESEARCH ARTICLE - ANTS

Ant assemblages (Hymenoptera: Formicidae) in three different stages of forest regenera-

tion in a fragment of Atlantic Forest in Sergipe, Brazil.
ECF Gomes, GT Ribeiro, TMS Souza, L Sousa-Souto
Universidade Federal de Sergipe (UFS), São Cristóvão, Sergipe, Brazil

Article History Abstract

In this study we compared the epigeic ant assemblages in forest fragments with three
Edited by
different status of plant recovery (an area reforested in 2007, another reforested in
Kleber Del-Claro, UFU, Brazil
Received 27 May 2014 2005 and another one of secondary forest, with over 35 years of plant regeneration),
Initial acceptance 10 June 2014 located in the municipality of Laranjeiras, Sergipe, Brazil. The ants were sampled in Febru-
Final acceptance 30 June 2014 ary (dry season) and June (rainy season) of 2012. We tested the following hypotheses: (1)
the species richness of ants increases with time after the process of forest restoration;
Keywords and (2) there are significant changes in species composition of ants among the three
bioindicators, degraded areas, envi-
stages of forest regeneration. Twenty-five pitfall traps were installed in each area. A
ronmental monitoring, species com-
position, Forest recovery. total of 82 morphospecies of ants were sampled, distributed in 31 genera and seven
subfamilies. The richness of ants was similar among the three sites (F = 1.71, p = 0.19).
Corresponding author The composition of ant species, however, was different in the area of late regeneration
Genésio Tâmara Ribeiro (35 years) compared to other areas of early reforestation (p <0.05). Thus, epigeic ants
Universidade Federal de Sergipe
were partially sensitive to changes in the habitat studied in response to reforestation,
Cidade Univ. Prof. José Aloisio de Campos
Av. Mal. Rondon, s/n, Jardim Rosa Elze presenting changes in species composition but no differences in ant species richness
São Cristovão-SE, Brazil among areas. We conclude that seven years after reforestation are not enough to re-
49100-000 store the same ant diversity in disturbed environments.
E-Mail: [email protected]

Introduction 1990; Folgarait, 1998). In tropical ecosystems the importance

of ants is more evident because they can represent up to 60%
Remaining forests are important for the maintenance of all arthropod biomass, and approximately 90% of their
of favorable environmental conditions for the establishment abundance (Hölldobler & Wilson, 1990; Floren & Linsen-
and persistence of native fauna (Gibson et al., 2011; Ulyshen, mair, 1997).
2011). Several studies have shown that part of the world- Species richness and structure of ant assemblages can
wide decline in biodiversity, threatening the functioning of be used as response variables in environmental monitoring, as
ecosystems, is related to anthropogenic modification of the these insects are sensitive to anthropogenic activities, includ-
landscape (Dirzo & Raven, 2003; Colombo & Joly, 2010; ing agricultural practices (Hernández-Ruiz & Castaño-Me-
Tabarelli et al., 2010), including the Atlantic Forest, one of neses, 2006) and reforestation (Pais & Varanda de 2010;
the main hotspots in the world (Myers et al., 2000). Schmidt et al., 2013). Therefore, the study of these insects
Deforestation of Atlantic Forest is considered a constant is useful to assess the success of forest restoration practices
threat to biological diversity (Melo et al., 2009; Oliveira et (Sobrinho et al., 2003; Silva & Silvestre, 2004; Holway &
al., 2004), including ant assemblages (Leal et al., 2012) and Suarez, 2006; Wetterer, 2012).
the monitoring of areas in process of plant recovery can be an Although recovery of degraded areas is commonly used
important tool in the diagnosis of these threats (Conceição et to reduce the negative environmental impacts on forest rem-
al., 2006; Delabie et al., 2006). nants (Metzger, 2009; Calmon et al., 2011) and, in spite of
Due to its abundance in most terrestrial ecosystems several studies on the role of the replanting of native species
ants are considered ecologically dominant and play com- in accelerating the recovery of degraded environments, there
plex ecological roles such as ecosystem engineers, predators, are still many questions about the time required for the re-
herbivores and seed dispersal agents (Hölldobler & Wilson, covering of ant fauna along a gradient of forest regeneration
Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology
ISSN: 0361-6525
Sociobiology 61(3): 250-257 (September 2014) 251

of fragments dominated previously by an agricultural matrix closed canopy (10°49’17”S; 37°11’13”W).

(Neves et al., 2010; Teodoro et al., 2010; Leal et al., 2012). Epigeic ants were sampled in 15 transects of 50 m,
Processes that influence the structure and species diver- being five transects per area. We established a minimum
sity of epigeic ants in agroecosystems are still poorly known distance of 150 m between each transect. Ant sampling was
(Neves et al., 2010; Teodoro et al., 2010), despite the increasing conducted using pitfall traps on the ground surface. In each
conversion of forest fragments in less diverse and structurally transect, five pitfalls were installed at a distance of 10 m, to-
simple habitats (Primack & Corlett, 2005; Barona et al., 2010). taling 25 pitfalls/site. Pitfalls consisted of 1,000 cm3 plastic
In this study, we investigated the response of epigaeic pots containing approximately 120 cm3 water with detergent
ant assemblages in forest fragments with three different sta- and were kept for 48 h in the field (Schmidt & Solar, 2010).
tus of plant recovery, aiming to test the following hypothe- Sampling was conducted in two periods, one during
ses: (1) Species richness of ants increases with time after the the dry season (February 2012) and another during the rainy
process of forest restoration (following an increase in habitat season (June 2012). All ants collected were sorted to species
complexity) and (2) the composition of ant species undergoes level when possible or morphospecies, using identification
changes along a gradient of regeneration of reforested area, keys from Bolton (1994) and Fernandez (2003) and later the
with reduction of generalist species. identification was confirmed through comparison with speci-
mens from the collection of the Laboratório de Ecologia de
Material and Methods Comunidades (Ant collection), of the Universidade Federal
de Viçosa and Laboratório de Mirmecologia of the CEPEC/
The study was conducted in three sites: two sites were CEPLAC, Ilhéus, Bahia, Brazil. Voucher specimens of all
previously plantations of sugar-cane that were reforested, one species are deposited in Laboratório de Pragas Florestais of
with 32ha in 2005 (RF1) and another with 30.7ha and re- the Universidade Federal de Sergipe.
forested with native species in 2007 (RF2). The third area is To verify the effect of habitat type (RF1, RF2, and FF)
a secondary Atlantic Forest fragment with 55ha ​​(FF) used as and sampling period (wet or dry season) (response variables)
“Area of ​​permanent preservation” (APP). All sites are located on the species richness of ants (explanatory variable) the linear
at Fazenda Boa Sorte, a large sugar-cane company, located in mixed effect (LME) was used, followed by residuals analy-
the municipality of Laranjeiras (10° 48’ 44”S, 37° 10’ 16” W), sis to verify the adequacy of the error distribution and the fit
state of Sergipe, Brazil. of the model. Fixed factors were sampling sites (RF1, RF2,
The studied region is dominated by agricultural land and FF), while samples (nested within sites) were treated as
with altitude ranging from 30 to 68 m a.s.l. The mean annual random factors. A minimum adequate model (MAM) was
temperature is 25.5 °C and annual average rainfall of 1,200 obtained by extracting non-significant terms (P < 0.05) from
mm. The rainy season usually lasts from May to October. The the full model arranged by all variables and their interaction
original vegetation was dominated by Atlantic forest and all (Crawley, 2007), using the software R (R Development Core
remnants are embedded in a 20 year-old, homogeneous ma- Team, 2009).
trix of sugar-cane fields (Cuenca & Mandarino, 2007). The A non-metric multidimensional scaling (NMDS) analy-
soil type is Spodozol, mainly sandy clay, deep, with low fer- sis was carried out to verify differences in the composition
tility and high porosity (draining rainfall). The area reforested of ant fauna among the forest regeneration types (Neves et
in 2005 (RF1) with 32 ha, is at an intermediate stage of devel- al., 2010). The ordination was conducted using the Jaccard
opment, with seven years of planting and composed of trees index. Additionally, similarity analysis (ANOSIM; Clarke,
with canopy of approximately 4-6 meters (10°49’15,8”S; 1993) were conducted to compare the difference between two
37°09’41”W). The other area, reforested in 2007 (RF2), with or more groups of sampling units among sites. Differences
30.7 ha is in early stage of development, with five years of between R-values were used to determine similarity patterns
planting and composed by sparse patches of woody vegeta- among ant assemblages in the three sites. The analysis were
tion, shrubs, herbs and grasses with a single layer of treetops conducted using the software PAST (Hammer et al., 2001).
with up to 4 m tall (10°49’01,6”S; 37°09’40,7”W).
Fourteen species of trees native to the Atlantic Forest Results
were used in reforestation: Tapirira guianensis, Caesalpinia
echinata, Genipa amerciana, Spondias lutea, Schinus terebin- We collected 82 ant morphospecies, distributed in 31
thifolius, Erythrina velutina, Enterolobium contorsiliquum, genera (Table 1). The subfamilies Myrmicinae and Formici-
Cleome tapia, Caesalpinia leiostachya, Inga marginata, Cas- nae presented 66% of all ant species sampled, with 42 and 12
sia grandis, Lonchocarpus sericeus, Anadenanthera macro- morphospecies, respectively. The genera Pheidole and Cam-
carpa and Hymenaea courbaril ponotus presented the higher richness with 11 (13.5%) and
The fragment (FF) of Atlantic Forest is an area of​​ 10 (12%) morphospecies, respectively. Twelve species were
secondary forest, protected from logging for over 35 years restricted to RF1 site, six species were found exclusively in
and consists of trees with 7-20 meters in height that forms a RF2 site while 34 species were restricted to FF site (Table 1).
252 ECF Gomes et al - Ant assemblages in a fragment of Atlantic Forest

Table 1. Relative frequency of epigeic ant species collected in pit- Table 1. (continued)
falls, during the wet and dry season of 2012 in three sites of different
Ant Subfamilies FF RF1 RF2
forest regeneration stages: a fragment of secondary forest (FF) one
area of reforestation with five years (RF2) and other with seven years Dry Wet Dry Wet Dry Wet
of reforestation (RF1). Trachymyrmex sp. 1 0.2 - - - - -
Occurrence in each season Monomorium floricula - - 0.2 - 0.8 -
Ant Subfamilies FF RF1 RF2 Solenopsis tridens - - 0.2 0.2 - -
Dry Wet Dry Wet Dry Wet Solenopsis sp. 2 0.2 0.6 - - - -
DOLICHODERINAE Solenopsis sp. 3 0.6 - - - - -
Dolichoderus lutosus - 0.2 - - - - Solenopsis saevissima 0.2 - 0.6 0.6 0.8 0.4
Dolichoderus diversus - 0.2 - - - - Solenopsis globularia - - 0.2 1 - 0.8
Dolichoderus attelaboides - 0.2 - - - - Hylomyrma balzani 0.2 0.2 - - - -
Dorymyrmex biconis - - - - 0.2 -
Pheidole radoszkowskii 0.4 0.4 1 1 0.6 1
Azteca sp. 1 0.8 0.4 - - - -
Pheidole fimbriata - - 0.2 0.4 - -
Azteca sp. 2 0.2 - - - - -
Pheidole (gr. Diligens) sp. 3 0.4 0.8 - - - -
Azteca sp. 3 - 0.2 - - - -
Pheidole sp. 4 0.6 1 - - - -
ECITONINAE
Pheidole (gr. Flavens) sp. 5 0.2 0.4 - 0.4 - -
Labidus praedator - 0.4 - - - -
Pheidole (gr. Tristis) sp. 6 0.8 0.4 0.2 - - -
Labidus coecus - - 0.4 - 0.4 -
Pheidole (gr. Fallax) sp. 7 - - 1 0.4 0.8 1
Nomamyrmex esenbeckii - - - 0.2 - -
Pheidole (gr. Diligens) sp. 8 - - - 0.2 1 0.2
Neivamyrmex diana - - - 0.2 - -
Pheidole sp. 9 - - - - - 0.4
FORMICINAE
Pheidole (gr. Fallax) sp. 10 - - 0.4 0.6 0.2 -
Brachymyrmex pr. patagonicus - - - 0.2 - -
Pheidole (gr. Fallax) sp. 11 0.6 0.8 0.8 0.4 0.8 0.4
Camponotus trapezoideus 0.2 - - - - -
Crematogaster abstinens - - 1 0.4 0.4 1
Camponotus renggeri 1 0.4 - - - -
Crematogaster sp. 2 - - 0.2 - - -
Camponotus bispinosus 0.2 - - - - -
Crematogaster pr. Distans - - - - 0.6 -
Camponotus novogranadensis 0.6 1 - - - -
Crematogaster sp. 4 0.4 - - - - -
Camponotus fastigatus 1 - - - - -
Crematogaster sp. 5 0.2 - - - - -
Camponotus arboreus 0.2 - 0.2 - - -
Cardiocondyla emeryi - - 0.2 - 0.2 -
Camponotus cingulatus 0.8 - - - - - PONERINAE
Camponotus vittatus - 0.4 0.8 1 0.6 0.8
Odontomachus haematodos 1 1 1 0.6 0.8 1
Camponotus (Myrmaphaenus) sp.9 - - 1 0.8 0.8 -
Leptogenys unistimulosa 1 0.6 0.6 0.8 1 0.4
Camponotus rufipes - - 0.4 - 0.2 1 Hypoponera sp. 1 0.2 - - - - -
Nylanderia pr. fulva - - 0.4 - 0.2 - Pachycondyla venerae 0.4 0.4 - - - -
MYRMICINAE Pachycondyla harpax 0.4 - - - 1 -
Piramica pr. perpava 0.4 0.4 - - - - ECTATOMMINAE
Piramica sp. 2 - 0.2 - - - - Gnamptogenys acuminata 0.2 - - - - -
Cephalotes atratus 0.6 - - - - - Gnamptogenys sulcata - - 0.4 - 0.4 -
Cephalotes umbraculatus 0.2 - - - - - Ectatoma bruneunn - - 0.4 - 0.6 0.6
Cephalotes minutus - - - 0.2 - - Ectatoma tuberculatum 0.2 - 0.6 0.2 - -
Cephalotes maculatus 0.2 - - - - - Ectatoma edentatum 0.4 0.8 0.2 0.6 - -
Cephalotes pusillus - - - 0.2 - - PSEUDOMYRMECINAE
Cephalotes depressus - - - - - 0.4 Pseudomyrmex tenuis 0.8 0.6 - - - -
Acromyrmex balsani - - 0.6 - 0.4 0.2 Pseudomyrmex termitarius - - 0.2 - 0.2 -
Acromyrmex rugosos rugosos - 0.6 0.4 0.2 0.2 - Pseudomyrmex sp. (gr. Pal-
- - - - 0.2 -
Atta sexdens rubropilosa - - 0.2 - 0.2 - lidus)

Cyphomyrmex minutus - 0.2 - - - - Pseudomyrmex sp. 4 - - - 0.4 - -

Cyphomyrmex transversus - - 0.6 0.2 0.8 0.4 Pseudomyrmex gracilis - - 0.2 - - -

Mycetosoritis sp. 1 * - - - - - 0.2 Pseudomyrmex sp. 6 - - 0.2 - - -

Mycocepurus obsoletus - 0.4 - - - - Pseudomyrmex sp. 7 - - 0.2 - - -

Sericomyrmex sp. 1 0.2 0.2 - - - - FF34 ve/ RF1.12 vd/ RF2.6 p/ Comuns30; * New genus sp.1, R.
Sericomyrmex sp. 2 - 0.4 - - - - Feitosa (personal communication, 19 September 2012) 
Sociobiology 61(3): 250-257 (September 2014) 253

There was no significant difference in species richness more complex areas and regenerating ones have been found
of ants among the three sites of forest regeneration (F2,22 = by other authors (Vasconcelos, 1999; Schmidt et al., 2013).
2.26, p = 0.12). However, the species richness of ants was In general, generalist species have higher colonization rate of
lower in the wet season in the RF1 and RF2 sites, compared disturbed fragments than do specialist ants (Schoereder et al.,
to FF area (F1,22 = 11.19, p = 0.002) (Fig.1). 2004).
The NMDS analysis indicates the formation of two dis- Although there were no differences in species richness
tinct groups (stress = 0.15) with one group represented by FF among sites, there were differences between season of sam-
and another group formed by RF1 And RF2 (Fig.2). Besides, pling, with higher values in the dry season of RF1 and RF2
the analysis of similarity (ANOSIM) indicated significant dif- (seasonality was not tested as a hypothesis in this study, and
ference in the structure of ant assemblages between FF versus thus we used this variable only as a source of variation in the
RF1 (p = 0.003) as well as FF versus RF2 (p = 0.001) (Table 2). statistical model).
The SIMPER analysis indicated that the morphospe-
cies that contributed most to the differentiation among sites Table 3. SIMPER Analysis among three sites of different forest re-
were Pheidole (group Fallax) sp.7, Camponotus (Myrma- generation stages: a fragment of secondary forest (FF) one area of
reforestation with five years (RF2) and other with seven years of
phaenus) sp 9, Crematogaster abstinens, Camponotus vit- reforestation (RF1).
tatus, Solenopsis saevissima, Pheidole sp. 4, Cyphomyrmex
transversus, Solenopsis globularia, Ectatoma edentatum, Species
Cumulative percent of dissi-
Camponotus renggeri and Pseudomyrmex tenuis. These mor- milarity (%)

phospecies together contributed to 31.5% of cumulative dis- Pheidole (group Fallax) sp.7 3.407
similarity among stages of plant recovery (Table 3). Camponotus (Myrmaphaenus) sp.9 6.709
Crematogaster abstinens 9.905
Table 2. Analysis of similarity (ANOSIM) among three sites of dif-
ferent forest regeneration stages: a fragment of secondary forest (FF) Camponotus vittatus 12.89
one area of reforestation with five years (RF2) and other with seven Solenopsis saevissima 15.77
years of reforestation (RF1).
Pheidole sp. 4 18.58

  FMN RF1 RF2 Cyphomyrmex transversus 21.25

FMN - 0.0003** 0.0001** Solenopsis globularia 23.92

RF1 0.0003** - 0.0732 Ectatoma edentatum 26.59

RF2 0.0001** 0.0732 - Camponotus renggeri 29.05

Pseudomyrmex tenuis 31.51
** significant difference, p< 0,01.

Discussion

In our study the species richness did not differ with time
of restoration and, on the one hand, it suggests that five years
are enough for the recovery of ant species richness. This time
can be considered short compared to that from other studies
conducted by Vasconcelos (1999) and Roth et al. (1994) (10
and 25 years, respectively). On the other hand, however, the
differences found in species composition among FF and RF1
or RF2 indicate that other parameters, rather than species rich-
ness, are important to make decisions about the use of ants as
bioindicators. An increase in species richness in FF might be cor-
related with a more complex environment, leading to an increase
in availability of resources (Matos et al., 1994, Oliveira et al., 1995).
The restoration of RF1 and RF2 sites with native species
of trees might have created favorable conditions for coloni-
zation of ants and have led to comparable values of species
Figure 1. Species richness of ants in the dry season (white bars) and
richness in FF area. The colonization of ants, however, seems rainy season (hatched bars) (mean ± SE) sampled in three areas with
to have been carried out by ant species from adjacent agro- different stages of forest recovery. RF1 = Fragment with 7 years of
ecosystems and not from nearby forested areas, since the reforestation; RF2 = Fragment of 5 years of reforestation and FF =
composition of species between FF and the other two areas forest fragment with 35 years of plant recovery (D and W indicate
differ greatly. Difference in ant species composition between sampling in dry and wet seasons, respectively). Different letters on
bars indicate significant difference within the same site (p <0.05).
254 ECF Gomes et al - Ant assemblages in a fragment of Atlantic Forest

for colonization in degraded areas. Other studies in the Atlan-

tic Forest recorded S. globularia in a disturbed mangrove area
(Delabie et al., 2006) and C. transversus in grasslands (Braga
et al., 2010). In fact, the areas RF1 and RF2 have low densi-
ty of tree species, allowing the establishment of herbaceous
species.
Individuals of Solenopsis saevissima exhibit aggres-
sive behavior and are also usually associated with disturbed
environments (Silvestre et al., 2003). The presence of this spe-
cies is favored in sites colonized by pioneer plant species,
typically found in early sucessional areas (Vasconcelos, 2008;
Schmidt et al., 2013). Although Camponotus vittattus was
sampled in all three areas, this species had similar occurrence
to S. saevissima being more frequent in samples from RF1 and
RF2, thus suggesting its preference for opened sites. In con-
trast, we also reported the presence of some ant species in sites
with late regeneration time (RF2 and FF), such as Ectatoma
Figure 2. Analysis of non-metric multidimensional scaling ordina- edentatum. Previous studies have associated the occurrence
tion (NMDS) from the assemblage composition of ants in three sites of this species with advanced stages of plant recovery (Ramos
of different forest regeneration stages: a fragment of secondary for- et al. 2003; Vasconcelos 2008).
est (FF) one area of reforestation with five years (RF2) and other
The RF1 site had a similar species richness of epigeic
with seven years of reforestation (RF1).
ants compared with RF2 or FF sites. However, the species
composition differs considerably among environments with
Changes in the frequency of foraging ants have been similar historical disturbances versus a forest fragment with
observed with environmental seasonality (Wolda, 1988; Kas- late regeneration. Our study shows that ant assemblages can
pari, 2000; Castro et al., 2011; Cook et al., 2011). The avail- vary greatly along a gradient of plant recovery and the conser-
ability of resources is reduced during the dry months of the vation of forest fragments with different stages of reforesta-
year, and the increased mobility of ants in this period might tion is important to sustain more diverse ant fauna. Therefore,
explain the rise in species richness in the dry season (Andow, reforestation programs that prioritize the conservation and
1991; Dantas et al., 2011). These results, however, should be the adoption of native plant species in these areas are a good
viewed with caution since the data were collected consider- alternative (Gillespie et al. 2000), enabling the development
ing just a year and a longer period of collection is needed to of scientific studies and especially the maintenance of local
establish more secure inferences about effects of seasonality biodiversity.
on ant species.
Considering that thirty-four species were restricted to Acknowledgments
FF site (42% of all species found) our results make it clear
that environmental differences among the areas were crucial The authors are grateful to Júlio Cezar Mário Chaul,
for determining the composition of species. Laboratory of Community Ecology - UFV and Jacques H. C.
The most common species in the FF were Camponotus Delabie, Laboratory of Myrmecology CEPEC / CEPLAC for
renggeri, Pheidole sp.4 and Pseudomyrmex tenuis, indicating their help in species identification. This study was supported
a preference of these species for less-disturbed environments. by the Coordenação de Aperfeiçoamento de Pessoal de Nível
Notably, several studies also demonstrate the occurrence of Superior (CAPES).
C. renggeri in seasonal forest formations such as Cerrado
(Del-Claro & Oliveira, 1999; Christianini et al., 2007; Neves References
et al., 2012) and forests in the semi-arid region of Brazil
(Hites et al., 2005). Conceição et al. (2006) also have report- Andow, D.A. (1991). Vegetational diversity and arthropod
ed the presence of P. tenuis in environments with low dis- population responses. Annual Review of Entomology, 36:
turbance. Besides, predatory species of the genus Pyramica 561-586.
(Masuko, 2009) were also found only in the FF, suggesting
that this fragment has a more suitable resource availability Barona, E., Ramankutty, N., Hyman, G. & Coomes, O. T.
than the other areas. (2010). The role of pastureand soybean in deforestation of the
The genera Pheidole (group Fallax) sp.7, Camponotus Brazilian Amazon.Environmentl Research Letters, 5: 1-9.
(Myrmaphaenus) sp.9, Crematogaster abstinens, Solenopsis Bolton, B. (1994). Identification guide to ant genera of the
globularia and Cyphomyrmex transversus, were found in RF1 world. Harvard University Press, Cambridge, 222p.
and RF2, indicating that these species could have preference
Sociobiology 61(3): 250-257 (September 2014) 255

Braga, D.L., Louzada, J.N.C., Zanetti, R. & Delabie, J. (2010). indicators of human impact in mangroves of the southeastern
Avaliação rápida da diversidade de formigas em sistemas de coast of Bahia, Brazil. Neotropical Entomology, 35: 602-615.
uso do solo no sul da Bahia. Ecology, Behavior and Bionomics,
Del-Claro, K. & Oliveira, P.S. (1999). Ant-Homoptera Inter-
39: 464-469.
actions in a Neotropical Savanna: The Honeydew-Producing
Calmon, M., Brancalion, P.H.S., Paese, A., Aronson, J., Treehopper, Guayaquila xiphias (Membracidae), and its As-
Castro, P., Silva, S.C. & Rodrigues, R.R. (2011). Emerging sociated Ant Fauna on Didymopanax vinosum (Araliaceae).
Threats and Opportunities for Large-Scale Ecological Resto- Biotropica, 31: 135-144.
ration in the Atlantic Forest of Brazil. Restoration Ecology,
Dirzo, R. & Raven, P.H. (2003). Global State of Biodiversity and
19: 154-158. doi: 10.1111/j.1526-100X.2011.00772.x.
Loss. Annual Review of the Environment and Resources, 28:
Castro, F.S., Gontijo, A.B., Castro, P.T.A. & Ribeiro, S.P. 137-167.
(2011). Annual and Seasonal Changes in the Structure of Lit-
Fernandez, F. (2003). Introducción a las hormigas de la region
ter-Dwelling Ant Assemblages (Hymenoptera: Formicidae) in
Neotropical. Acta Noturna, Bogotá, 398pp.
Atlantic Semideciduous Forests. Psyche, vol. 2012, Article ID
959715, 12 pages, 2012. doi:10.1155/2012/959715 Floren, A. & Linsenmair, K.E. (1997). Diversity and recolo-
nization dynamics of selected arthropod groups on different
Christianini, A.V., Nunes, A.J.M. & Oliveira, P.S. (2007). The
tree species in a lowland rainforest in Sabah, with special ref-
role of ants in the removal of non-myrmecochorous diaspo-
erence to Formicidae. Canopy Arthropods (eds N.E. Stork, J.
ras and seed germination in a neotropical savanna. Journal of
Adis & R.K. Didham). pp. 344–381, Chapman & Hall, Lon-
Tropical Ecology, 23: 343-351.
don.
Clarke, K.R. (1993). Non-parametric multivariate analysis of
Folgarait, P.J. (1998). Ant biodiversity and its relationship to
changes in community structure. Austral Ecology, 18: 117-
ecosystem functioning: a review. Biodiversity and Conserva-
143.
tion, 7: 1221-1244.
Colombo, A.F. & Joly, C.A. (2010). Brazilian Atlantic Forest
Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A.,
lato sensu: the most ancient Brazilian forest, and a biodiversi-
Barlow, J., Peres, C.A., Bradshaw, C.J.A., Laurance, W.L.,
ty hotspot, is highly threatened by climate change. Brazilian
Lovejoy, T.E. & Sodhi, N. (2011). Primary forests are irre-
Journal of Biology, 70: 697-708.
placeable for sustaining tropical biodiversity. Nature, 478:
Conceição, E.S., Costa-Neto, A.O., Andrade, F.P., Nascimen- 378-383. doi:10.1038/nature10425.
to, I.C., Martins, L.C.B., Brito, B.N., Mendes, L.F. & Delabie,
Gillespie, T.W., Grijalva, A. & Farris, C.N. (2000). Diversity,
J. (2006). Assembléias de Formicidae da serapilheira como
composition, and structure of tropical dry forests in Central
bioindicadores da conservação de remanescentes de Mata
America. Plant Ecology, 147: 37-47.
Atlântica no extremo sul do Estado da Bahia. Sitientibus Série
Ciências Biológicas, 6: 296-305. Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001). PAST: Pa-
laeonthological Statistics Software Package for education and
Cook, S.C., Eubanks, M.D., Gold, R.E. & Behmer, S. T.
data analysis. Palaeontologia Electronica, 4: 1-9.
(2011). Seasonality Directs Contrasting Food Collection
Behavior and Nutrient Regulation Strategies in Ants. PLoS Hernández-Ruiz, P. & Castaño-Meneses, G. (2006). Ants
ONE, 6: 1-8. (Hymenoptera: Formicidae) diversity in agricultural ecosys-
tems at Mezquital Valley, Hidalgo, Mexico. European Journal
Crawley, M. J. (2007). The R Book. John Wiley & Sons Ltd,
of Soil Biology, 42: 208-212.
England, 950p.
Hites, N.L., Mourao, M.A.N., Araujo, F.O., Melo, M.V.C., Bi-
Cuenca, M. A. G.& Mandarino, D. C. (2007). Mudança da
seau, J.C. & Quinet, Y. (2005). Diversity of the ground-dwell-
Atividade Canavieira nos Principais Municípios Produtores
ing ant fauna (Hymenoptera: Formicidae) of a moist, montane
do Estado de Sergipe de 1990 a 2005. Documentos 122, Em-
Forest of the semi-arid Brazilian “Nordeste”. Revista de Bio-
brapa Tabuleiros Costeiros, 22p.
logia Tropical, 53: 165-173.
(Disponível em HTTP://<www.cpatc.embrapa.br>).
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Harvard
Dantas, K.S.Q., Queiroz, A.C.M., Neves, F.S., Júnior, R.R. &
University Press, Massachusetts, Cambridge. 732p.
Fagundes, M. (2011). Formigas (Hymenoptera: Formicidade)
em diferentes estratos numa região de transição entre os bio- Holway, D. A. & Suarez, A. V. (2006). Homogenization of
mas do Cerrado e da Caatinga no norte de Minas Gerais. MG ant communities in mediterranean California: The effects
Biota, 4: 17-36. of urbanization and invasion. Biological Conservation, 127:
319-326.
Delabie, J.H.C., Paim, V.R.L.D.M., Nascimento, I.C.D.,
Campiolo, S. & Mariano, C.D.S.F. (2006). Ants as biological Kaspari, M. (2000). A primer of ant ecology. In: Agosti, D. &
Alonso, L. (Eds.), Measuring and monitoring biological di-
256 ECF Gomes et al - Ant assemblages in a fragment of Atlantic Forest

versity, standard methods for Ground-living Ants (pp. 9-24). cal Computing, Vienna, Áustria, 409 pp.
Washington: Smithsonian Institution Press.
Ramos, L.D., Filho, R.Z.B., Delabie, J.H.C., Lacau, S., Santos,
Leal, I.R., Filgueiras, B.K.C., Gomes, J.P., Lannuzzi, L. & M.F.S., Nascimento, I.C. & Marinho, C.G. (2003). Ant com-
Andersen, A.N. (2012). Effects of habitat fragmentation on munities (Hymenoptera: Formicidae) of the leaf-litter in cer-
ant richness and functional composition in Brazilian Atlantic rado “stricto sensu” areas in Minas Gerais, Brazil. Lundiana,
forest. Biodiversity Conservation, 21: 1687-1701. 4: 95-102.
Masuko, K. (2009). Studies on the predatory biology of Ori- Roth, D.S., Perfecto, I. & Rathcke, B. (1994). The effects
ental dacetine ants (Hymenoptera: Formicidae) II. Novel prey of management systems on ground-foraging ant diversity in
specialization in Pyramica benten. Journal of Natural History, Costa Rica. Ecological Applications, 4: 423-436.
43: 13-14.
Schmidt, F.A. & Solar, R. R.C. (2010). Hypogaeic pitfall
Matos, J.A., Yamanaka, C.N., Castellani, T.T. & Lopes B.C. traps: methodological advances and remarks to improve the
(1994). Comparação da fauna de formigas de solo em áreas de sampling of a hidden ant fauna. Insectes Sociaux, 57: 261-266.
plantio de Pinus elliottii, com diferentes graus de complexi-
Schmidt, F.A., Ribas, C.R. & Schoereder, J.H. (2013). How
bilidade estrutural (Florianópolis, SC.). Biotemas, 7: 57-64.
predictable is the response of ant assemblages to natural forest
Melo, F.V., Brown, G.G., Constantino, R., Louzada, J.N.C., recovery? Implications for their use as bioindicators. Eco-
Luizão, F.J., Morais, J.W. & Zanetti, R.A. (2009). A importân- logical Indicators, 24: 158-166.
cia da meso e macrofauna do solo na fertilidade e como bi-
Schoereder, J.H.;  Sobrinho, T.G.;  Ribas, C. R. &  Campos,
ondicadores. Boletim Informativo da SBCS. (Disponível em
R.B.F. (2004). Colonization and extinction of ant communi-
http://<sbcs.solos.ufv.br/solos/boletins/biologia%20macro-
ties in a fragmented landscape. Austral Ecology, 29: 391-398.
fauna.pdf.>).
Silva, R.R. & Silvestre, R. (2004). Diversidade de formigas
Metzger, J.P. (2009). Conservation issues in the Brazilian At-
(Hymenoptera: Formicidae) que habita as camadas superfici-
lantic forest. Biological Conservation, 142: 1138-1140.
ais do solo em Seara, Oeste de Santa Catarina. Papéis Avulsos
Myers, N., Mittermeier R.A., Mittermeier C.G, Fonseca de Zoologia, 44: 1-11.
G.A.B. & Kent, J. (2000). Biodiversity hotspots for conserva-
Silvestre, R.C., Brandão, C.R.F. & Silva, R.R. (2003). Grupos
tion priorities. Nature, 403: 853-858.
funcionales de hormigas: el caso de los gremios del Cerrado.
Neves, F.S., Braga, R.F., Araujo, L.S., Campos, R.I. & Fagundes, In F. Fernández (Ed.). Introducción a las hormigas de la re-
M. (2012). Differential effects of land use on ant and herbi- gión neotropical (pp. 113-148). Bogotá: Acta Nocturna.
vore insect communities associated with Caryocar brasiliense
Sobrinho, T.G., Schoereder, J.H., Sperber, C.F. & Madureira,
(Caryocaraceae). Revista de Biologia Tropical, 60: 1065-1073.
M.S. (2003). Does fragmentation alter species composition in
Neves,F.S., Braga,R.F., Espírito-Santo, M.M., Delabie, Ant communities (Hymenoptera: Formicidae)? Sociobiology,
J.H.C., Fernandes, G.W. & Sanchez-Azofeifa, G. A.(2010). 42: 329-342.
Diversity of arboreal ants an a Brazilian Tropical Dry Forest:
Tabarelli, M., Aguiar, A.V., Ribeiro, M.C., Metzger, J.P. &
Efects of seasonality and successional Stage. Sociobiology,
Peres, C.A. (2010). Prospects for biodiversity conservation
56: 177-194.
in the Atlantic Forest: Lessons from aging human-modified
Oliveira MA, Grillo AA, Tabarelli M (2004). Forest edge in landscapes. Biological Conservation, 143: 2328-2340.
the Brazilian Atlantic Forest: drastic changes intree species
Teodoro, A. V., Sousa-Souto, L., Klein, A.M. & Tscharntke,
assemblages. Oryx, 38: 389–394.
T. (2010). Seasonal contrasts in the response of coffee ants
Oliveira, M.A., Della-Lucia, T.M.C., Araújo, M.S. & Cruz, to agroforestryshade-tree management. Environmental Ento-
A.P. (1995). A fauna de formigas em povoamentos de euca- mology, 39:1744-1750.
lipto na mata nativa no estado do Amapá. Acta Amazonica,
Ulyshen, M.D. (2011). Arthropod vertical stratification in
25: 117-126.
temperate deciduous forests: Implications for conserva-
Pais, M.P. & Varanda, E.M. (2010). Arthropod Recolonization tion-oriented management. Forest Ecology and Management,
in the Restoration of a Semideciduous Forest in Southeastern 261: 1479-1489.
Brazil. Neotropical Entomology, 39: 198-206.
Vasconcelos, H. L. (1999). Effects of forest disturbance on
Primack, R.B. & Corlett, R.T. (2005). Tropical Rain Forests: the structure of ground-foraging ant communities in central
An Ecological and Biogeographical Comparison. Blackwell Amazonia. Biodiversity and Conservation, 8: 409-420.
Science, Oxford. 336p.
Vasconcelos, H.L. (2008). Formigas do solo nas florestas da
R Development Core Team. (2009). R: A language and envi- Amazônia: padrões de diversidade e respostas aos distúrbios
ronment for statistical computing. R Foundation for Statisti- naturais e antrópicos. In: Moreira, F.M., Siqueira, J.O. &
Sociobiology 61(3): 250-257 (September 2014) 257

Brussaard, L. Biodiversidade do solo em ecossistemas brasi- ing ant, Cardiocondyla emeryi (Hymenoptera: Formididae).
leiros (pp. 323-343). Lavras: Editora UFLA. Mymercological News, 17: 13-20.
Wetterer, J.K. (2012). Worldwide spread of Emery’s sneak- Wolda, H. (1988). Insect seasonality: why? Annual Review of
Ecology and Systematics, 19: 1-18.