PsycheVolume 2012 (2012), Article ID 636749, 23 pagesdoi:10.1155/2012/636749

Review Article

Ants as Indicators in Brazil: A Review with Suggestions to Improve the Use of Ants in Environmental Monitoring Programs

Carla R. Ribas,¹ Renata B. F. Campos,² Fernando A. Schmidt,³ and Ricardo R. C. Solar³

¹Laboratory of Ant Ecology, Sector of Ecology, Department of Biology, Federal University of Lavras, 37200-000 Lavras, MG, Brazil²Institute of Education of Divinópolis, Educational Foundation of Divinópolis, 35501-170 Divinópolis, MG, Brazil³Post-Graduate Program in Entomology, Department of Entomology, Federal University of Viçosa, 36570-000, Viçosa, MG, Brazil

Received 31 May 2011; Revised 11 August 2011; Accepted 16 August 2011

Academic Editor: Jonathan D. Majer

Copyright © 2012 Carla R. Ribas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

We describe the use of ants as indicators in Brazil, based on a critical review of published articles. The analysis of fifty-eight papers, encompassing a range of almost 25 years, indicates an increased number of studies using ants as indicators in the last decade. Among the parameters analyzed in the papers, species composition is the most suitable to evaluate the effect of the disturbance on ant communities. The use of other metrics that consider the specificity and fidelity (e.g., IndVal index) of ant species to a level or state of disturbance is also highly desirable. We discuss several alternative ways of overcoming many of the drawbacks related to the robustness of the results and to reduce the financial, logistic, and time costs involved with the use of ants as indicators in monitoring programs. By doing so, we expect to encourage new research on ants as bioindicators as well as to summarize current knowledge, facilitating further research.

1. Introduction

Intensive exploitation of natural resources and the resulting impacts on pristine habitats have led to calls from the scientific community and the general public to measure or monitor the level of these environmental impacts [1–3]. Bioindicators are a useful way to evaluate such impacts, since changes in their population dynamics or community parameters can indicate an environmental state more easily, quickly, and safely and with lower financial and labour inputs than direct measurements [4–6].

McGeoch [7] divided the general use of the term bioindication into three categories according to the three main applications: (i) environmental indicators: used to detect or monitor changes in the environmental state, (ii) ecological indicators: used to demonstrate the impact of an environmental stress on the biota or monitor longer-term stress-induced changes in the biota, and (iii) biodiversity indicators: used to identify the diversity of a taxa in a specified area or to monitor changes in biodiversity.

Therefore, there are several characteristics that an indicator species must have, the most notable being ease of measurement, sensitivity to environmental stress, and predictable responses to environmental stress [4, 8]. The use of certain species or groups of species as indicators of successful rehabilitation practices or for environmental monitoring has been recommended in recent years (e.g., [5, 6, 9]).

Ants have been used as a powerful tool in several ecological studies [10, 11]. This group has useful characteristics for successful indication and monitoring of environmental impacts, including widespread distribution, high abundance, importance in ecosystem functioning, ease of sampling, and relatively well-known taxonomy and ecology [12].

Thus, ants have been used as indicators of several environmental impacts, such as fire, deforestation and logging, agricultural intensification, mining, and urbanization [13, 14]. The first study suggesting the use of ants as indicators was in the early 1980s [15], and the use of ants as indicators is now widespread in Australia (e.g., [16–19]) and is becoming a major focus of myrmecological research worldwide (e.g., [20–25]).

Although ants are a simple, cheap, and powerful indicator of environmental impacts and rehabilitation (e.g., in Australia [17]), in Brazil, a country which harbours enormous diversity and complexity of habitats, the standard use of ants as indicators is still relatively new and should be evaluated in greater detail (see [26, 27]). According to Philpott et al. [14] and Gardner [6], a critical need is the selection of ant species that are affected by distinct types of disturbance in different regions, in order to guarantee their usefulness as good indicators.

Therefore, as we described above, given the international use of ants as indicators, several studies have investigated the use of ants as indicators in Brazil. In order to describe the background of bioindication with ants in Brazil, we carried out a critical review of several studies concerned directly or indirectly with the use of ants as indicators.

Using the three categories proposed by McGeoch [7], environmental, ecological, or biodiversity indicators, we describe the historical development of ants as indicators and evaluate the implications of these studies. Additionally, we highlight ways of overcoming the major challenges to the widespread use of ants as tools in environmental monitoring programs.

2. Methods

We searched for papers regarding ants as indicators, restricting our search to those carried out in Brazil. To encompass a broad time range of papers, we used the following keywords in Portuguese and English, respectively: “formiga,” “ant,” “indicador,” “bioindicador,” “indicator,” “bioindicator,” “Brasil,” “Brazil,” and the combination of the words cited above in the Scielo and in the ISI Web of Knowledge websites. We also used papers from our personal archives, gathered under several keywords.

In all papers, we accessed the following information: the language, the general idea of the paper (i.e., descriptive, a general survey, a test of correlations or hypotheses), if the paper specifically analyzed ants as indicators; the aims; the ant sampling methodology, the parameters of ant fauna which were analyzed (i.e., diversity, composition, population dynamics), the environmental parameters which were observed, the results which were obtained, and the main conclusion reached in the study.

We define the paper as specifically analyzing ants as indicators if it explicitly declared this intention in the aim or the introduction (Explicit indication papers). However, if this criteria was not clear but the article still analyzed ants as indicators, we defined these as “Implicit indication papers.” Papers in which the major aim was not the use of ants as bioindicators, but which presented results that could Potentially enable the use of ants as indicators, were considered as “Potential indication papers.” Finally, papers that did not meet any of the above criteria, that is, did not mention in any way the use of ants as indicators, or with results that could not be used to evaluate ants as indicators, were considered as “Indirect bioindication papers.”

The disturbances or aims investigated in the papers were split into the categories “Agriculture,” “Vegetation type,” and “Human land-use,” according to the habitats studied, namely: habitats with agricultural activities only, habitats with natural vegetation only, and habitats with both agricultural activities and natural habitats. Similarly, “Succession” studies were those investigating natural succession, and “Restoration” studies were those evaluating different rehabilitation techniques, such as succession following managed restoration efforts.

We used McGeoch [7] as a reference to decide if the ants were used as environmental, ecological, or biodiversity indicators in the reviewed papers (see McGeoch’s [7] definition in the introduction section). Moreover, we defined ant species as indicators when there was a species list in the paper showing the occurrence of ants in specific sites or when the author considered the ant species to be an indicator elsewhere in the paper. If the ant species occurred in just one habitat, we considered the species to be an indicator of the specific habitat.

We verified the most frequent responses of ants to disturbance, summarizing responses, and relating the most frequent responses to the most frequently used sampling methodologies to determine if there were any trends. To study this relationship, we considered only methodologies that had been used in at least three papers.

3. Results

We analyzed 58 papers, which encompassed a span of almost 25 years (from 1987 to 2010). Among the papers, only one was not classed as an “indication paper” or “Potential indication paper” [83]. The others specifically mentioned the intention to use ants as indicators (either explicitly, using the word “indicator,” or implicitly, using ants as a tool or model to indicate the ecological and environmental parameters) (38 papers) or at least have the Potential to do so (17 papers) (Table 1). Two papers [84, 85] were not included in the table because the scope of the papers was not to analyse ants as indicators but to suggest new tools to simplify their use as indicators.

Table 1: Papers reviewed regarding ants as indicators in Brazil, indicating the main disturbance investigated (Disturbance), the aim of the paper (Aim), if the paper was explicitly, implicitly or has the Potential to be used in indicator studies (Indication), the environmental parameters analyzed/sampled (Environmental parameters), the responses of ant community to disturbance that were found to be significant (Effects on ant community), the indicator type used (Indicator type) and the paper (Reference).

Disturbance
Aim
Indication
Environmental parameters
Effects on ant community
Indicator type
Reference

Agriculture
Evaluate the effect of different soil tillage and crop management systems on soil fauna groups
Yes (implicit)
Soil tillage and crop management systems
Change in species dominance (discriminant and correspondence analysis)
Environmental
Baretta et al. [28]

Agriculture
Evaluate the ant diversity in fig crops under different managements
Yes
Types of soil cover plants
Change in density of species (, Tukey test)
Environmental
Merlim et al. [29]

Agriculture (forestry practices in Eucalyptus)
Use the ant guild concept to evaluate changes in Eucalyptus plantations following control of leaf-cutting ants
Yes
Forestry practices
Change in species composition—observed frequency of species and guilds (non-statistical test)
Environmental
Lacau et al. [30]

Agriculture (preceded by deforestation and fire)
Assess the recolonization by fauna in areas cleared and burned to plant corn and beans
Yes
Human land-use and resting time
Increase in abundance in the less-disturbed areas (non-statistical test)
Environmental
Nunes et al. [31]

Agriculture (formicid granulated baits)
Evaluate the effect of different applications of formicide baits on nontarget ant community
Yes
Forms and timing of application of formicid-granulated baits
No effect of bait type on ant species richness (, ANOVA) Reduction in species richness observed only in control method, systematic application being more harmful (, ANOVA)
Environmental
Ramos et al. [32]

Anthropogenic activities
Quantify heavy metals in worker ants of Camponotus rufipes collected in different environments
Yes
Observed human interference
Three groups of ants with different heavy metal concentrations (PCA analyses)
Environmental
Silva et al. [33]

Conservation status
Create an inventory of epigaeic ant species that occur in vine forest and use them to indicate the level of conservation of this ecosystem
Yes
None
Inventory (nonstatistical test)
—
Carvalho et al. [34]

Conservation status
Verify the impact of human use in mangroves
Potential
Observed levels of human use
Reduction on species richness
Environmental
Delabie et al. [35]

Conservation status
Inventory the ant community in the Baturité hills
Yes
None
Inventory (nonstatistical test)*
—
Hites et al. [36]

Conservation status
Study the ant communities in preserved and impacted savanna sites
Yes
Observed human interference
Reduction of diversity in impacted sites *
Environmental
Ramos et al. [37]

Fire
Test the negative effect of fire in Restinga environments on the ant community
Potential
Presence of fire
Increase in species richness with presence of fire (mean and confidence intervals of estimated species richness)
Environmental
Endringer et al. [38]

Fire
Test the hypothesis that ant species richness and composition change after burning sand dunes
Yes
History of fire
More ant species and distinct species composition in the unburned area (non-statistical test)
Environmental
Teixeira et al. [39]

Fragmentation
Verify the responses of ants nesting in twigs in the litter layer to habitat changes associated with forest fragmentation
Potential
Distance to forest edge, remnant isolation, leaf-litter depth, density of dead twigs, and vegetation (three parameters measured)
Higher species richness ; most ant species had greater nest densities in continuous areas than in remnants, change in species composition with forest edge
Ecological
Carvalho and Vasconcelos [40]

Fragmentation
Determine the effect of forest fragmentation on ant communities
Yes
Remnant area, distance to forest edge, vegetation cover of matrix, and vegetation (three parameters measured)
No effect of many fragment characteristics on ant species richness: area , distance core-border . Only tree density had an effect
Ecological
Gomes et al. [41]

Fragmentation
Know the community of ants in forest fragments
Yes
Remnant area
No change in species richness with remnant area *
Environmental
Santos et al. [42]

Forestry systems
Describe the epigaeic ant communities in Eucalyptus plantations
Yes
Eucalyptus age
No change in species richness with Eucalyptus age
Environmental
Fonseca and Diehl [43]

Human land-use
Compare the ant community structure between a crop and a secondary forest
Potential
Land use
Reduction of diversity and equitability and change in species composition (non-statistical test)
Environmental
Castro and Queiroz [44]

Human land-use
Compare the impact of different agroecosystems on ant species richness
Yes
Land use
Higher species richness in forest edges and pasture (non-statistical test); coffee crop presented reduced estimated richness
Environmental
Dias et al. [45]

Human land-use
Survey of ant and termite fauna in four patches with different vegetation structures and in one open field
Potential
Land use
Change in species richness and composition (non-statistical test)
Environmental
Diehl et al. [46]

Human land-use
Test the effects of Restinga soil characteristics on ant communities
Yes (implicit)
Land use, physical and chemical soil properties, and microbial activity
Change in species richness (non-statistical test) and composition (canonical correspondence analysis)
Ecological
Gomes et al. [47]

Human land-use
Elucidate ant species richness and community structure associated with the micro basin of Sanga Caramuru-Chapecó
Yes
Habitat type, temperature, and rainfall
Change in species composition (Bray-Curtis Cluster Analysis indicated higher similarity for disturbed areas) and higher richness (observed and estimated) in the native area (sample-based accumulation curves)*
Environmental
Ilha et al. [48]

Human land-use
Determine the level of similarity of ant communities in forest areas (three native forest remnants) and an Eucalyptus reforestation
Yes
Land use
Change in species composition (Jaccard index— among Eucalyptus crops versus forest remnants and among forest remnants)
Environmental
Lapola and Fowler [49]

Human land-use
To inventory the ant fauna in a Cerrado area and in Eucalyptus plantations with five classes of understory ages
Yes
Eucalypt age
Higher density of species in Cerrado areas than in Eucalyptus (non-statistical test) and estimated species richness similar between areas
Environmental
Marinho et al. [50]

Human land-use
Investigate the effect of structural characteristics of the environment on ant communities
Yes
Habitat type
Change in species richness and composition (non-statistical test)
Environmental
Santana-Reis and Santos [51]

Human land-use
Test the hypotheses that there was a decrease in ant species richness and a change in the species composition in habitats with more intense soil use
Yes
Land use
Sites with distinct soil use host a differential ant species composition (cluster analysis-Euclidean distance)
Environmental
Schmidt and Diehl [52]

Human land-use
Evaluate the effect of collection time (day and night) on ant fauna attracted to baits in areas of Eucalyptus cloeziana (Myrtaceae) and Cerrado (savanna vegetation)
Potential
Land use
Collection time effect was more important to ant fauna structure than the vegetation effect (ordination analyses)
Environmental
Tavares et al. [53]

Human land-use and succession
Compare ant diversity under different land-use systems
Yes
Land use and age of succession
Change in density of species (non-statistical test), species richness (sample-based accumulation curves and χ2), and composition (cluster analysis)*
Environmental
Braga et al. [54]

Inundation
Document the ant fauna in three different forest types (one annually inundated and two on terra firme)
Potential
Vegetation (several parameters measured)
Change in diversity, similarity, and proportion of different nesting and feeding habitats (non-statistical test)
Ecological
Majer and Delabie [55]

Logging
Test the hypothesis that logging affects forest ant fauna by reducing the species richness and changing the composition of ground-foraging ant communities
Yes
Canopy openness, abundance of understory vegetation, and leaf-litter depth
Change in species composition proportion of Pheidole was reduced from 21.4% and 26% in unlogged forest and low-impact logging, respectively, to 14.8% in high-impact logging
Ecological
Kalif et al. [56]

Mining
Determine the levels of heavy metals in plants and identify soil organisms of the mesofauna that could be biological indicators of soil quality
Yes
Physical and chemical soil properties and heavy metal content
Decrease in abundance and increase in lead (Pb) accumulation (non-statistical test)
Environmental
Barros et al. [57]

Mining
Ant fauna survey and community structure, analyses of the ground-dwelling ants in native vegetation and areas with different inferred copper levels
Yes
Areas with different inferred copper levels
Decrease in species richness with inferred copper levels (non-statistical test)
Environmental
Diehl et al. [58]

Restoration (agriculture)
Investigate the recolonization profile of the restored Atlantic Forest
Yes
Age after planting
Increase in species richness (, ANOVA) and change in species composition (ANOSIM, )*
Environmental
Pais and Varanda [59]

Restoration (anthropogenic disturbance)
Test the hypothesis that ant fauna is closely related to the structural complexity of habitat
Yes
Age of restoration
Change in species composition (non-statistical test)
Environmental
Coelho et al. [60]

Restoration (dredging disturbance)
Evaluating ant bioindication of impacted habitats
Yes
Time since restoration, distance from the impact, and physical properties of soil
Change in species richness: higher in cerrado than in the restoration habitats, and also higher in the ecotone and intermediate zones than on the beach and change in abundance and composition (non-statistical test)
Environmental
Costa et al. [61]

Restoration (mining)
Investigate which ants recolonized reclaimed areas in subtropical regions and evaluate the effect of different rehabilitation techniques, comparing results with Australia
Yes
Age of rehabilitation, soil penetrability, number of logs, litter and vegetation measures (three and five parameter, resp.)
Increase in species richness (non-statistical test) and change in composition (PCoA)
Ecological
Majer [62]

Restoration (mining)
Evaluate the efficacy of rehabilitation procedures in mining sites on facilitating ant recolonization and compare it with other tropical regions and climatic zones
Yes
Age of restoration, soil penetrability, litter depth, percentage of litter, grass, and herb cover, and vegetation (several parameters measured)
Species richness increased in early ages but slowed in late ages and was smaller than control site (non-statistical test). Distinct species composition in sites at early ages, intermediate ages, and control sites (ordination analyses)
Ecological
Majer [63]

Restoration (mining)
Investigate the community structure changes of different rehabilitation techniques
Yes
Rehabilitation technique
Change in species richness (non-statistical test) and composition (cluster analysis)
Ecological
Pereira et al. [64]

Road
Test the hypothesis that dirt roads are favourable landing sites for Atta laevigata founding queens. Analyze the importance of litter cover as a proximate cue in nest-site selection
Potential
Presence of dirt roads
The number of colonization attempts in roads was 5 to 10 times greater than that in the adjacent vegetation
Environmental
Vasconcelos et al. [65]

Seasonality
Investigate ant diversity and species composition on an island
Yes
Seasonality
Change in species richness and composition with seasonality (non-statistical test)*
Environmental
Schmidt et al. [66]

Succession
Examine whether secondary forests of the Brazilian Atlantic Forest act as refugia for forest-adapted species
Yes (implicit)
Age of succession and soil type
Richness and composition of ant assemblages in secondary forests have recovered slowly and have not approached conditions typical to old-growth forests
Environmental
Bihn et al. [67]

Succession
Examine bait preferences of litter ants along a successional gradient of forest
Potential
Age of succession
Preference of ants for the type of bait changed along the successional gradient . In young successional stages, N baits attracted more ants than CHO baits, whereas in late successional stages, CHO baits attracted more ants
Environmental
Bihn et al. [68]

Succession
Investigate how functional diversity profile changed in a successional gradient
Potential
Age of succession
Increased diversity and change in functional groups (non-statistical test)
Environmental
Bihn et al. [69]

Succession
Verify patterns in the structure of ant communities along a successional gradient
Potential
Age of succession
Increased diversity and equitability (non-statistical test)
Environmental
Castro et al. [70]

Succession
Compare ant diversity among sites in different successional stages
Potential
Age of succession
Higher diversity in intermediary stage and change in composition (non-statistical test)
Environmental
Leal et al. [71]

Succession
Compare the diversity and composition of tree-dwelling ants in different successional stages of a seasonal deciduous forest
Potential
Age of succession
Increase in species abundance and change in species composition (PCA analysis)
Environmental
Neves et al. [72]

Succession
Compare the ant species diversity related to successional stage and seasonality
Yes
Age of succession, tree richness and density
Change in species composition (DCA deterrent correspondence analysis, )
Ecological
Neves et al. [73]

Succession
Evaluate the long-term effect of fire on ant species richness
Potential
Presence of fire 15 years before
Change in species composition (cluster analyses-Euclidean distance)
Environmental
Santos et al. [74]

Succession
Assess the changes in species richness and composition between relatively pristine habitat and along a forest regeneration gradient
Yes
Age of succession
Increase in species richness (sample-based accumulation curves) and distinct species composition between pristine area and areas at regeneration (ANOSIM, *
Environmental
Silva et al. [75]

Succession
Compare the structure of the ground ant communities in areas at different levels of restoration
Yes
Age of succession
Increase in species richness and decrease in abundance , change in species composition (ordination analysis)
Environmental
Vasconcelos [76]

Succession
Determine experimentally the effects of selective logging on ground-living ants
Yes
Logging age, canopy cover, litter depth, and understory density
Species richness, evenness, and abundance per plot did not vary among treatments . Most of the species found in the control plots were also present in the logged plots
Ecological
Vasconcelos et al. [77]

Urbanization
Compare the thermal tolerances of leaf-cutter ants (Atta sexdens) from colonies inside and outside an urban area
Potential
Temperature
Urban ants support higher temperatures better than rural ones, which present higher rates of mortality
Environmental
Angilletta et al. [78]

Vegetation type
Inventory ants
Yes
Habitat type
Change in species richness (non-statistical test)*
Environmental
Diehl et al. [79]

Vegetation type
Test how the diversity of one taxa can be a good surrogate of all diversity
Yes
Habitat type
Correlation with other taxa (Pearson correlation coefficients)
Biodiversity
Leal et al. [80]

Vegetation type
Compare ant diversity in three different forest stages (primary, reforestation, and secondary)
Potential
Habitat type
Change in diversity and exclusive species (non-statistical test)*
Environmental
Lopes et al. [81]

Vegetation type
Compare the ant fauna from forests and nearby patches of savanna (Cerrado) in the Brazilian Amazon. Assess whether there is a difference in the fauna between the ground and lower vegetation strata in both habitats
Potential
Habitat type
Forests host twice as many species as savanna (sample-based rarefaction curves). In both habitats, the ground hosted more species than vegetation (). Distinct species composition between forest and savanna and between ground and vegetation within the same habitat; ant species fidelity and specificity is given by IndVal (see Table 2)
Environmental
Vasconcelos and Vilhena [82]

*papers with sample-based accumulation curves.

From the 58 papers, exactly half (29) were published in English and the other half in Portuguese. Among the “Potential indication papers,” 11 were published in English and six in Portuguese, while among the “indication papers” the number of papers written in Portuguese (22) was higher than the papers written in English (18).

Papers directly concerned with the use of ants as bioindicators began almost 10 years after the development of “Potential indication papers”, in which the main focus was the response of ant communities to several disturbances (e.g., logging and land use). Only in the last decade has there been a positive trend of papers using ants as model organisms for bioindication in Brazil (Figure 1).

Figure 1: Trend of the number of analyzed papers regarding ants as indicators in Brazil. Indication papers—paper specifies (explicitly or implicitly) the intention of analyzing ants as indicators in the aim or introduction. Potential indication paper—the above criteria was not met, but the paper presents results that could potentially enable the use of ants as indicators.

Regarding ant sampling procedures, 34 studies used only a single sampling method: 14 used two, six used three, and four opted for more than three methods. The methodologies used to capture ants were baits, beating, Berlese extraction, hand collecting, pitfall traps, sweeping, Tretzel traps and Winkler’s extractors. Among these methodologies, the most commonly used were baits (used in 26 studies), followed by hand collecting, pitfall traps and Winkler’s extractors (used in 20 studies each), and Berlese extraction (used in five studies).

The majority of studies sampled ants at the soil surface (44), but some studies also considered the soil surface together with other habitats, including litter (10), vegetation (7), combination of the above (6). Some other studies did not sample ants at the soil surface, but only in the litter (11), vegetation (two), or in twigs (one), respectively.

The main impacts studied were succession (12), human land-use (11), restoration (6), and agriculture (5). Just a few papers (13) analyzed other environmental parameters besides disturbance (Table 1).

The parameters of the ant faunas that were most commonly related to the disturbance type were ant species richness or diversity indexes (42) and species composition (35) (Table 1). In these papers, if we considered only those that analyzed ant species diversity and composition rigorously (i.e., with statistical tests), the actual number of papers that analyzed ant species diversity decreased to 28, and those that analyzed ant species composition dropped to 22.

Regarding species composition, in 33 papers this parameter was sensitive to disturbance, although if we considered only those papers with statistical analyses, the number decreases to 21. Summarizing the papers that analyze species richness or diversity, the responses found were species richness or diversity increased with disturbance (1), decreased with disturbance (18), changed with disturbance (when there is any clear trend in the response of ants to disturbance) (11), and not affected by disturbance (12). If we considered only papers that tested ant species richness or diversity statistically, the numbers changed to increase with disturbance (1), decrease with disturbance (11), change with disturbance (5), and not affected by disturbance (11).

By connecting the main responses found in the papers (ant species richness, diversity, or ant species composition) to the main methodologies used to sample ants, we can verify some trends (Figure 2). First, species composition was sensitive to disturbance in the majority of papers in which this parameter was tested, irrespective of the sampling methodology, namely, baits plus hand collecting, multiple sampling methods, or pitfall traps. Second, most papers that analyzed species richness or diversity showed that these metrics were also responsive to disturbance, although the sole use of baits or the Winkler did not show any trend, while only using pitfall traps revealed a positive response of ant species richness or diversity to disturbance. Nevertheless, when we considered only those papers with statistical tests (Figure 3) or without statistical tests (Figure 4), the trend for species composition remained the same, but for species richness the use of multiple methods to sample ants showed a higher number of responses to disturbance.

(a)

(b)

Figure 2: Papers that analyzed (a) ant species composition and/or (b) ant species richness/diversity with and without statistical tests and their responses to habitat disturbance through the use of different ant sampling methodologies. Composition changed—species composition altered by disturbance. Composition not changed—species composition not altered by disturbance. S increased—species richness or diversity increased with disturbance. S not altered—species richness or diversity not affected by disturbance. S decreased—species richness or diversity decreased with disturbance. S changed—species richness or diversity changed with disturbance when there is any clear trend in the response of ants to disturbance.

(a)

(b)

Figure 3: Papers that analyzed (a) ant species composition and/or (b) ant species richness/diversity with statistical tests and their responses to habitat disturbance through the use of different ant sampling methodologies. Composition changed—species composition altered by disturbance. Composition not changed—species composition not altered by disturbance. S increased—species richness or diversity increased with disturbance. S not altered—species richness or diversity not affected by disturbance. S decreased—species richness or diversity decreased with disturbance. S changed—species richness or diversity changed with disturbance when there is any clear trend in the response of ants to disturbance.

(a)

(b)

Figure 4: Papers that analyzed (a) ant species composition and/or (b) ant species richness/diversity without statistical tests and their responses to habitat disturbance through the use of different ant sampling methodologies. Composition changed—species composition altered by disturbance. Composition not changed—species composition not altered by disturbance. S increased—species richness or diversity increased with disturbance. S not altered—species richness or diversity not affected by disturbance. S decreased—species richness or diversity decreased with disturbance. S changed—species richness or diversity changed with disturbance when there is any clear trend in the response of ants to disturbance.

The ants were used as environmental indicators in the majority of studies (42 out of 55) but were also used as ecological indicators (10 papers) and as biodiversity indicators in only one paper. In 20 papers there was a species list, and; therefore, we could determine some of the ant species that served as indicators of certain habitats. The parameters used in the papers to define a species as an indicator were frequency of ant occurrence (11 papers), presence or absence of ant species (8 papers), and the indicator value (IndVal) (1 paper). Irrespective of the parameter used by the authors, 187 ant species were defined as indicators and linked to specific habitats (Table 2). The genera with higher numbers of indicator species were Camponotus (18), Pseudomyrmex (12), Pachycondyla (11), Ectatomma (9), Gnamptogenys (9), Acromyrmex (8), and Cephalotes (8). The sites with the most indicator species were forest (39 species), Eucalyptus (37), savanna (34), control or undisturbed sites (nonburnt) (29), primary forest (25), early succession sites (19), disturbed sites (15), secondary forest (14), intermediate succession sites (13), burnt sites, low human land-use-impacted sites and pasture (9), late succession (8), and strong human land-use-impacted sites (5).

Table 2: Species of ants defined as indicators, indicating the parameter used by the authors (Parameter) when linking each ant species to each habitat type (Habitat) and the paper (Reference).

Ant species
Parameter
Habitat
Reference

Acanthognathus brevicornis
Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Acanthognathus ocellatus
Frequency of occurrence
Primary forest
Silva et al. [75]

Acanthognathus rudis
Frequency of occurrence
Primary forest
Silva et al. [75]

Acanthoponera mucronata
Frequency of occurrence
Native forest remnant
Ilha et al. [48]

Acromyrmex balzani
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Presence/absence
Undisturbed sites—control site
Diehl et al. [58]

Acromyrmex coronatus
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Acromyrmex lobicornis
Presence/absence
Undisturbed sites—control site
Diehl et al. [58]

Acromyrmex lundi
Frequency of occurrence
Secondary forest
Schmidt and Diehl [52]

Acromyrmex niger
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Acromyrmex rugosus
Frequency of occurrence
Turnera ulmifolia field
Santana-Reis and Santos [51]

Acromyrmex striatus
Presence/absence
Undisturbed sites—control site
Diehl et al. [58]

Acromyrmex subterraneus
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Acromyrmex subterraneus brunneus
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Acromyrmex subterraneus subterraneus
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Acropyga decedens
Frequency of occurrence
Pasture
Dias et al. [45]

Amblyopone armigera
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Presence/absence
Savanna—cerrado sensu stricto
Marinho et al. [50]

Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Amblyopone elongata
Frequency of occurrence
Primary forest
Silva et al. [75]

Anochetus diegensis
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Anochetus mayri
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Anochetus neglectus
Frequency of occurrence
Pasture
Dias et al. [45]

Anochetus targionii
Frequency of occurrence
Pasture
Dias et al. [45]

Apterostigma acre
Frequency of occurrence
Forest fragment
Dias et al. [45]

Apterostigma bolivianum
Frequency of occurrence
Forest fragment
Dias et al. [45]

Atta robusta
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Atta sexdens rubropilosa
Presence/absence
Area at early succession
Coelho et al. [60]

Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Azteca alfari
Presence/absence
Area at late succession stage—dry season
Neves et al. [73]

Azteca muelleri
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Basiceros disciger
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Blepharidatta brasiliensis
Frequency of occurrence
Area at late succession stage
Vasconcelos [76]

Brachymyrmex coactus
Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Camponotus arboreus
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Camponotus atriceps
Presence/absence
Reforestated area at intermediate succession stage
Coelho et al. [60]

Camponotus bidens
Presence/absence
Low human land-use-impacted sites
Delabie et al. [67

Camponotus burtoni
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Camponotus claviscapus
Presence/absence
Undisturbed sites
Delabie et al. [35]

Camponotus crassus
Presence/absence
Burned restinga
Endringer et al. [38]

Frequency of occurrence
Burnt site
Teixeira et al. [39]

Frequency of occurrence
Disturbed sites
Diehl et al. [58]

Frequency of occurrence
Secondary forest and forest edge
Leal et al. [71]

IndVal
Savanna—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Camponotus  fastigatus
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Camponotus  latangulus
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Presence/absence
Savanna—cerrado sensu stricto
Marinho et al. [50]

Camponotus leydigi
Frequency of occurrence
Area at early succession
Vasconcelos [76]

Camponotus melanoticus
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Pasture
Dias et al. [45]

Presence/absence
Area at early succession
Coelho et al. [60]

Camponotus novogranadensis
Frequency of occurrence
Area at early succession
Vasconcelos [76]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

IndVal
Forest—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Camponotus punctatus minutior
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Camponotus renggeri
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Camponotus rufipes
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Camponotus sericeiventris
Frequency of occurrence
Native forest remnant
Ilha et al. [48]

Camponotus trapezoideus
Frequency of occurrence
Burnt site
Teixeira et al. [39]

Frequency of occurrence
Forest fragment
Dias et al. [45]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Camponotus  vitatus
Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Camponotus westermanni
Presence/absence
Strong human land-used-impacted sites
Delabie et al. [35]

Cardiocondyla obscurior
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Carebara urichi
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Cephalotes  atratus
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

IndVal
Forest—vegetation stratum
Vasconcelos and Vilhena [82]

Cephalotes grandinosus
Presence/absence
Forest
Lopes et al. [81]

Cephalotes minutus
Presence/absence
Area at early succession—dry season
Neves et al. [73]

Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Cephalotes pallidicephalus
Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Cephalotes pavonii
Frequency of occurrence
Burnt site
Teixeira et al. [39]

Cephalotes pellans
Presence/absence
Area at intermediate succession—wet season
Neves et al. [73]

Cephalotes pusillus
IndVal
Savanna—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Cephalotes simillimus
IndVal
Savanna—vegetation stratum
Vasconcelos and Vilhena [82]

Crematogaster brasiliensis
IndVal
Forest—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Crematogaster erecta
Presence/absence
Area at intermediate succession
Coelho et al. [60]

IndVal
Savanna—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Crematogaster limata
IndVal
Forest—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Crematogaster minutissima
IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Crematogaster nigropilosa
Frequency of occurrence
Native forest remnant
Ilha et al. [48]

Crematogaster quadriformis
IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Cyphomyrmex laevigatus
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Cyphomyrmex major
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Cyphomyrmex olitor
Frequency of occurrence
Primary forest
Silva et al. [75]

Cyphomyrmex peltatus
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Forest fragments
Dias et al. [45]

Cyphomyrmex plaumanni
Frequency of occurrence
Primary forest
Silva et al. [75]

Cyphomyrmex salvini
Frequency of occurrence
Area at early succession
Vasconcelos [76]

Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Cyphomyrmex transversus
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Discothyrea sexarticulata
Frequency of occurrence
Forest fragment
Dias et al. [45]

Frequency of occurrence
Primary forest
Silva et al. [75]

Dolichoderus attelaboides
IndVal
Forest—vegetation stratum
Vasconcelos and Vilhena [82]

Dolichoderus bispinosus
IndVal
Forest—vegetation stratum
Vasconcelos and Vilhena [82]

Dolichoderus schulzi
Presence/absence
Undisturbed sites
Delabie et al. [35]

Dolichoderus voraginosus
Presence/absence
Area at early succession—dry season
Neves et al. [73]

Dorymyrmex guianensis
IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Dorymyrmex pyramicus
Frequency of occurrence
Burnt site
Teixeira et al. [39]

Presence/absence
Undisturbed sites
Delabie et al. [35]

Dorymyrmex thoracicus
IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Eciton quadriglume
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Ectatomma brunneum
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Area at early succession
Braga et al. [54]

Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Ectatomma edentatum
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Ectatomma lugens
Frequency of occurrence
Area at late succession stage
Vasconcelos [76]

IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Ectatomma muticum
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Ectatomma opaciventre
IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Ectatomma permagnum
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Frequency of occurrence
Eucalyptus forestry
Braga et al. [54]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Ectatomma planidens
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Ectatomma quadridens
Frequency of occurrence
Area at early succession
Vasconcelos [76]

Ectatomma tuberculatum
Frequency of occurrence
Area at early succession
Silva et al. [75]

Presence/absence
Burned restinga
Endringer et al. [38]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Area at late succession stage
Braga et al. [54]

Frequency of occurrence
Secondary forest and forest edge
Leal et al. [71]

Forelius maranhoensis
IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Gnamptogenys acuminata
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Gnamptogenys continua
Frequency of occurrence
Primary forest
Silva et al. [75]

Gnamptogenys horni
Frequency of occurrence
Area at late succession stage
Vasconcelos [76]

Gnamptogenys mediatrix
Frequency of occurrence
Forest fragment
Dias et al. [45]

Gnamptogenys moelleri
Frequency of occurrence
Pasture
Dias et al. [45]

Frequency of occurrence
Secondary forest and area at early succession
Schmidt and Diehl [52]

Gnamptogenys reichenspergeri
Frequency of occurrence
Primary forest
Silva et al. [75]

Gnamptogenys striatula
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Gnamptogenys sulcata
Presence/absence
Area at early succession—wet season
Neves et al. [73]

Gnamptogenys tortuolosa
Frequency of occurrence
Intermediate disturbed area
Vasconcelos [76]

Heteroponera flava
Frequency of occurrence
Forest fragment
Dias et al. [45]

Heteroponera microps
Frequency of occurrence
Disturbed habitat (Eucalyptus)
Ilha et al. [48]

Hylomyrma balzani
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Hylomyrma reitteri
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Hypoponera foeda
Frequency of occurrence
Native forest remnant
Ilha et al. [48]

Hypoponera foreli
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Hypoponera opacior
Frequency of occurrence
Disturbed habitat (Eucalyptus)
Ilha et al. [48]

Labidus coecus
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Presence/absence
Undisturbed sites
Delabie et al. [35]

Labidus praedator
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Secondary forest
Schmidt and Diehl [52]

Leptogenys pusilla
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Leptothorax asper
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Leptothorax spininodis
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Linepithema humile
Frequency of occurrence
Burnt site
Teixeira et al. [39]

Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Megalomyrmex goeldii
Frequency of occurrence
Area at early succession
Silva et al. [75]

Mycetagroicus cerradensis
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Mycetarotes paralelus
Presence/absence
Area revegetated with native species
Pereira et al. [64]

Mycetophylax conformis
Presence/absence
Strong human land-used-impacted sites
Delabie et al. [35]

Myrmicocrypta foreli
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Neivamyrmex orthonotus
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Nesomyrmex spininodis
Presence/absence
Strong human land-used-impacted sites
Delabie et al. [35]

Octostruma balzani
Frequency of occurrence
Area at intermediate succession
Braga et al. [54]

Octostruma jheringhi
Frequency of occurrence
Forest fragment
Dias et al. [45]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Odontomachus affinis
Frequency of occurrence
Secondary forest
Silva et al. [75]

Odontomachus bauri
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Odontomachus brunneus
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Odontomachus caelatus
Frequency of occurrence
Area at late succession stage
Vasconcelos [76]

Odontomachus chelifer
Frequency of occurrence
Pasture
Braga et al. [54]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Frequency of occurrence
Secondary forest and area at early succession
Schmidt and Diehl [52]

Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Odontomachus haematodus
Frequency of occurrence
Area at intermediate succession
Braga et al. [54]

Presence/absence
Burned restinga
Endringer et al. [38]

Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Odontomachus meinerti
Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Oxyepoecus plaumanni
Frequency of occurrence
Primary forest
Silva et al. [75]

Oxyepoecus rastratus
Frequency of occurrence
Primary forest
Silva et al. [75]

Pachycondyla apicalis
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pachycondyla arhuaca
Frequency of occurrence
Area at late succession stage
Braga et al. [54]

Presence/absence
Primary restinga
Endringer et al. [38]

Pachycondyla bucki
Frequency of occurrence
Primary forest
Silva et al. [75]

Pachycondyla crassinoda
IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Pachycondyla ferruginea
Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Pachycondyla gilberti
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pachycondyla harpax
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Pachycondyla obscuricornis
Frequency of occurrence
Eucalyptus (reforestation)
Lapola and Fowler [49]

Pachycondyla stigma
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Frequency of occurrence
Primary forest
Braga et al. [54]

Pachycondyla striata
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Presence/absence
Savanna—cerrado sensu stricto
Marinho et al. [50]

Frequency of occurrence
Secondary forest and area at early succession
Schmidt and Diehl [52]

Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Pachycondyla villosa
Presence/absence
Burned restinga
Endringer et al. [38]

Frequency of occurrence
Disturbed savanna
Ramos et al. [37]

Paratrechina longicornis
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Presence/absence
Undisturbed sites
Delabie et al. [35]

Pheidole diligens
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Pheidole embolopyx
Frequency of occurrence
Area at late succession stage
Vasconcelos [76]

Pheidole exigua
IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Pheidole fimbriata
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Presence/absence
Savanna—cerrado sensu stricto
Marinho et al. [50]

Pheidole fracticeps
IndVal
Forest—ground stratum
Vasconcelos and Vilhena [82]

Pheidole radoszkowskii
Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Pheidole scalaris
Presence/absence
Area at early succession—wet season
Neves et al. [73]

Pogonomyrmex abdominalis
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pogonomyrmex naegelii
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Prionopelta punctulata
Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Pseudomyrmex elongatus
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Pseudomyrmex filiformis
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Pseudomyrmex flavidulus
IndVal
Savanna—vegetation stratum
Vasconcelos and Vilhena [82]

Pseudomyrmex gracilis
Presence/absence
Area at intermediate succession
Coelho et al. [60]

IndVal
Savanna—vegetation stratum
Vasconcelos and Vilhena [82]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pseudomyrmex kuenckeli
Presence/absence
Undisturbed sites
Delabie et al. [35]

Pseudomyrmex oculatus
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

IndVal
Forest—vegetation stratum
Vasconcelos and Vilhena [82]

Pseudomyrmex schuppi
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Pseudomyrmex sericeus
Presence/absence
Undisturbed sites
Delabie et al. [35]

Pseudomyrmex simplex
Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pseudomyrmex spiculus
Presence/absence
Undisturbed sites
Delabie et al. [35]

Pseudomyrmex tenuis
Frequency of occurrence
Area at early succession
Vasconcelos [76]

IndVal
Forest—vegetation and ground stratum
Vasconcelos and Vilhena [82]

Presence/absence
Strong human land-use-impacted sites
Delabie et al. [35]

Frequency of occurrence
Area at intermediate succession
Braga et al. [54]

Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Pseudomyrmex termitarius
Presence/absence
Area at early succession—dry season
Neves et al. [73]

Frequency of occurrence
Pasture
Braga et al. [54]

IndVal
Savanna—vegetation stratum
Vasconcelos and Vilhena [82]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Pyramica appretiata
Frequency of occurrence
Primary forest
Silva et al. [75]

Pyramica denticulata
Frequency of occurrence
Area at early succession
Silva et al. [75]

Pyramica lygatrix
Frequency of occurrence
Primary forest
Silva et al. [75]

Pyramica rugithorax
Frequency of occurrence
Primary forest
Silva et al. [75]

Pyramica schulzi
Presence/absence
Strong human land-use-impacted sites
Delabie et al. [35]

Pyramica subdentata
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Frequency of occurrence
Secondary forest and area at early succession
Silva et al. [75]

Pyramica zeteki
Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Sericomymex bondari
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Presence/absence
Low human land-use-impacted sites
Delabie et al. [35]

Simopelta curvata
Frequency of occurrence
Pasture (edge)
Dias et al. [45]

Solenopsis geminata
Frequency of occurrence
Area at early succession
Vasconcelos [76]

Frequency of occurrence
Caesalpinia echinata forest
Santana-Reis and Santos [51]

Solenopsis saevissima
Frequency of occurrence
Disturbed sites
Ilha et al. [48]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

Solenopsis substituta
Frequency of occurrence
Burnt site
Teixeira et al. [39]

Presence/absence
Eucalyptus forestry
Marinho et al. [50]

IndVal
Savanna—ground stratum
Vasconcelos and Vilhena [82]

Sphinctomyrmex stali
Frequency of occurrence
Primary forest
Silva et al. [75]

Stegomyrmex vizzotoi
Frequency of occurrence
Primary forest
Silva et al. [75]

Strumigenys denticulata
Frequency of occurrence
Intermediate disturbed area
Vasconcelos [76]

Strumigenys elongata
Frequency of occurrence
Area at early succession
Silva et al. [75]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Strumigenys perparva
Presence/absence
Savanna—cerrado sensu stricto
Marinho et al. [50]

Frequency of occurrence
Preserved savanna
Ramos et al. [37]

Tapinoma melanocephalum
Frequency of occurrence
Disturbed habitat (Eucalyptus)
Ilha et al. [48]

Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Trachymyrmex cornetzi
Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Trachymyrmex fuscus
Frequency of occurrence
Pasture (edge)
Dias et al. [45]

Trachymyrmex zeteki
Frequency of occurrence
Primary forest
Silva et al. [75]

Typhlomyrmex major
Frequency of occurrence
Forest fragments
Lapola and Fowler [49]

Frequency of occurrence
Primary forest
Silva et al. [75]

Typhlomyrmex pusillus
Frequency of occurrence
Primary forest
Silva et al. [75]

Wasmannia auropunctata
Presence/absence
Area at intermediate succession
Coelho et al. [60]

Frequency of occurrence
Control site (nonburnt)
Teixeira et al. [39]

Wasmannia rochai
Presence/absence
Area at early succession
Coelho et al. [60]

4. Discussion

It has been possible to determine the history of research carried out in Brazil by searching for the use of ants as indicators over the last 25 years (Figure 1). From 1987 to 1991, there were only “Potential indication papers.” In 1992 the first “Indication papers” were published, which increased in the following years and exceeded the “Potential indication papers” in 2001.

Regarding the idiom of the papers, it is interesting to observe that half of the papers are still published in Portuguese. In spite of the growing internationalization of Brazilian research [86, 87], many Brazilian studies that use ants as bioindicators cannot have an international impact since they are in Portuguese. We determined at least two main reasons for this. The first is the “publish or perish” policy in Brazilian (and worldwide) science, which demands the publication of as many papers as possible in the shortest feasible time span, in which case publishing in Portuguese can be a way to speed up publication time. The second explanation may be that, due to problems with the style of writing of the papers, many international journals reject Brazilian papers. Despite these two issues, in this historical scenario, there is an improving and maturing of bioindication studies using ants, which is shown by the explicit use of the term “indication” in these papers. Furthermore, the increasing knowledge exchange with researchers from other countries reinforces the maturation of this area of research. Examples include Brazilian scientists that complete their Ph.D. studies abroad the possibility for doctorate students to undertake international exchange programs, and the internationalization of the Brazilian Symposium of Myrmecology.

However, it is important to clarify that although some authors explicitly used the term indicator in the introduction or in the aim of their papers (our criteria defined these papers as “Indication papers”), the authors did not always in reality use ants as indicators, either because they did not sample properly (i.e., sampling in just one habitat, without different levels of the disturbance/restoration and control sites) or because they did not analyze their results rigorously (i.e., did not include a satisfactory statistical analysis). Conversely, some authors did not use the term indicator in their papers, but they did test the Potential use of ants as indicators, and were cautious in the above points.

The majority of articles that used ants as environmental indicators (sensu [7]) may be due to the fact that this is the simplest way to detect a change in the environmental state of the habitat but not necessarily the best one. The use of ecological indicators has the advantage of encompassing a broad response as they demonstrate the disturbance effect on the biota, not only for ants [6].

Moreover, the sampling of different environmental parameters and their correlation with the biota is essential, because their inclusion increases the predictive power of the study. If we recognize the environmental parameters that are most sensitive to disturbance and their effect on the biota, we may be able to more accurately monitor the effects of disturbance. Consequently, we may be able to choose the restoration effort according to the most appropriate or effective environmental parameters in order to promote the recovery of the biota [6, 7].

Regarding the number of ant sampling techniques used, although the majority of the papers used only one method, several studies (e.g., [52, 77, 88]) have highlighted the fact that ant communities show a pronounced vertical stratification, and ant faunas specific to each microhabitat may present specific ecological traits and distinct sensitivity to the same environmental impact [67, 89–91]; therefore, more than one sampling method must be considered [13]. On the other hand, the use of several sampling methods increases the financial costs and the time needed to collect, sort, and process the data [13]. Thus, since environmental monitoring programs usually have short-term goals, it is desirable to balance the benefits and costs of using several types of sampling methods compared to using only one sampling method which could achieve similar reliable results (Figures 2(a) and 2(b)), compare multiple sampling and pitfall outcomes) about the patterns and aims under investigation.

The most used sampling method in the studies was attractive baits, which are more suitable for behavioural questions [92] and are useful for verifying the presence and population trends of invasive and keystone ant species [13]. However, this sampling method results in biased information about ant diversity (e.g., species richness and composition) because many ants have selective diets, and some ants can dominate the baits to the exclusion of a broad range of other ant species [92]. This notion concerning the use of baits in bioindication papers is confirmed in Figures 3(a) and 3(b), which shows that the sole use of baits revealed apparently unchanging species composition and no trend in species richness. Thus, Underwood and Fisher [13] recommend the use of pitfall traps and litter sampling (The Winkler and/or Berlese extractors) as effective ant sampling methods for monitoring goals related to the effect of habitat disturbance and transformation on ant diversity, which is corroborated in Figures 3(a), 3(b), 4(a), and 4(b).

Species richness and diversity and species composition are the parameters of ant communities most commonly analyzed in the papers. However, species richness and diversity should be used as an evaluative method with caution, since several studies have shown that these parameters were not affected by disturbance (Table 1), and only a narrow number of papers showed a trend in the response of ant species richness to disturbance (see Figures 3 and 4). This coarse relationship of species richness to disturbance is probably because ants are generalists, so the loss of some sensitive species to disturbance is compensated by the invasion of other opportunist species or more generalists. Moreover, in dynamic sites under frequent habitat transformation and disturbance, there is no change in species richness among sites at different restoration times, because perturbation events “reset” the ant community to the same stage [93].

In this way, as Hoffmann [94] has highlighted, the disturbance induced changes in species composition, but not necessarily in species richness. Moreover, the recovery of species composition takes longer than species richness [95] and has a strong relation to the vegetation structure [19, 64, 96–99], which changes with disturbance events. Thus, species composition should be a better parameter to evaluate the effect of disturbance on ant communities, even in areas with frequent perturbations, as described by Gollan et al. [93].

Using the same argument, the quantification of the relationship between each ant species and different disturbances (or level of disturbance) or habitats should be very useful, as it is important to decrease the time spent in indication studies. The general public and stakeholders need to know rapidly if the habitat is impacted or recovering, so recognizing which species can be associated positively or negatively with disturbance or restoration is a very desirable tool.

Several of the papers we analyzed described species occurring exclusively or more frequently in specific habitats (Table 2), but we are concerned with the lack of rigour with which this has been carried out in most studies (exception in [82]), as there is no control about the specificity and fidelity of these ant species and few statistical analyses to validate the results. This lack of rigour may explain why there are some ant species with contradictory patterns of occurrence, such as species being present in disturbed versus undisturbed sites, such as Acromyrmex balzani, Camponotus trapezoideus, Dorymyrmex pyramicus, Ectatomma tuberculatum, Odontomachus haematodus, and Pseudomyrmex tenuis (see Table 2). Moreover, these ant species might also be generalists, and the choice of better criteria should enable us to distinguish between inappropriate sampling design and truly generalist ant species. The use of the IndVal index [8], mentioned below, is one option to overcome this drawback.

The Indicator Value (IndVal) suggested by Dufrêne and Legendre [8] combines a measure of the habitat specificity of a species to a level of disturbance, or to a disturbance state, with its fidelity within that state. The random reallocation procedure of samples within sample groups can be used to test the significance of the IndVal measure for each species. The use of this method has increased (e.g., [100–105]) and has a number of advantages over other methods [6].

Some species seem to have more consistent responses to disturbance or specificity to some habitats, but this consistency is very difficult to assert due to the lack of rigour with which the ants were related to disturbance or habitats (presence or frequency of occurrence) and the lack of standardization regarding the level of disturbance in the papers. The habitats sampled in one paper may be defined as undisturbed, which may be different from the habitats studied in another paper that are defined as more degraded (or less) and should also be defined as an undisturbed habitat. In our paper (including Table 2), we used the definition of disturbed or undisturbed given by the original authors.

Thus, following the disturbance definition used by the authors, some species are present in disturbed habitats in more than one paper, and, therefore, could be indicators of disturbed habitats, such as Atta sexdens rubropilosa, Camponotus crassus, Camponotus melanoticus, Camponotus novogranadensis, Odontomachus meinerti, Pachycondyla villosa, Pseudomyrmex termitarius, and Solenopsis saevissima. In the same way, some species could be indicators of undisturbed habitats, such as Labidus coecus, Pachycondyla arhuaca, Pachycondyla stigma, and Sericomymex bondari. There are also some species that are indicators of specific habitats, such as indicators of forests (Discothyrea sexarticulata, Ectatomma lugens, Labidus coecus, and Typhlomyrmex major) and indicators of savannas (Camponotus latangulus, Pheidole fimbriata, and Strumigenys perparva).

One of the major mistakes related to the use of a taxon as an indicator is the personal motivation of the researchers. There are two ways of avoiding this mistake; several taxa should be rigorously tested a priori to select the best one [4] or studied a posteriori to validate the response of the indicator [7]. Very few studies have compared how different taxa, including ants, perform under different disturbances (see [89, 101, 106–109]).

The majority of studies end at the seventh step of the “Procedural steps in bioindicator studies” according to McGeoch [7], which is “Based on the nature of the relationship, either accept or reject the species, higher level taxon or assemblage as an indicator,” and just investigate the nature of the relationship between the disturbance and the indicator. To validate the organism as a suitable indicator, we must move to step eight (Establish the robustness of the indicator by developing and testing appropriate hypotheses under different conditions)—establish the robustness of the indicator by testing the same relationship in other areas or at different times (to validate the indicator) [6, 14, 103].

We would like to flag some issues to improve and validate the use of ants as indicators in environmental monitoring programs, including consideration of robust criteria for the validation of ants as indicators, sampling in different seasons and under different disturbances with comparable methodologies, collecting ants with different sampling methodologies in order to recognize that the responses of different ant life styles could be different for the same disturbance, and evaluation of different environmental parameters (biotic and abiotic) to correlate with the ants’ response along the disturbance/restoration gradients. The search for indicator ant species should be with analyses that consider their fidelity and specificity to the habitats (e.g., “IndVal” index), in order to more quickly achieve monitoring goals. Finally, evaluating the functional loss of ant species in disturbed habitats will improve predictions about the functional implication of the disturbance.

Moreover, incorporating new approaches that efficiently simplify the study may help to decrease the problems related to time spent identifying ant species, as suggested by Groc et al. [85]. In this study, the authors introduced a new method based on mixed-level taxonomic sufficiency, highly focused on higher-taxon surrogacy. Under this method, only ant species pre established as “indicator taxa” must be taxonomically identified to species level, while other species may be identified to higher (and easier to identify) levels, such as genera. By using this mixed-level approach, the authors argue that a considerable improvement in cost effectiveness can be achieved, mainly by reducing the necessity for well-trained taxonomists to be involved in the study. This is highly desirable in monitoring programs, where time and budget are key limiting factors.

Also, species which have been identified as possible indicators because they occur in specific habitats or conditions still require validation for reliable use as bioindicators, and their presence or frequency in specific conditions can generate testable hypothesis about their relationship with these habitats and conditions, which in turn can validate the use of these species as bioindicators.

In conclusion, we point out that the use of ants as indicators in Brazil has been improving each year. Ants are a useful tool not only because they are sensitive to environmental changes, as related in the papers we reviewed but also because they are keystone species in several ecological processes and, therefore, provide reliable inferences about the ecological and functional implications of disturbances.

We should continue to study ants in Brazil, with proper a priori hypothesis tests and sampling designs, statistical analysis and standardized methods, in order to reach the same widespread acceptance of ants as indicators that is common in Australia, as well as to improve our understanding of ant dynamics for predictive frameworks. Moreover, we need to build an effective bridge between our accumulated knowledge (almost 25 years of research) of ants as bioindicators and monitoring programs developed to examine natural resources and areas.

Acknowledgments

This study resulted from the research project: CRA 270/07 “Utilização de formigas como bioindicadoras de impacto ambiental e de sua recuperação em Cerrado e em Mata Atlântica.” The authors are grateful to Jacques H. C. Delabie for encouraging the elaboration of this paper, to Jonathan D. Majer for his kind attention in providing several papers and to Patty Ramirez for her valuable suggestions in the English expression. The authors received grants and funding from the FAPEMIG, CAPES, and CNPq.

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