Psyche: A Journal of Entomology

Psyche: A Journal of Entomology / 2012 / Article
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Advances in Neotropical Myrmecology

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Review Article | Open Access

Volume 2012 |Article ID 636749 | 23 pages | https://doi.org/10.1155/2012/636749

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

Academic Editor: Jonathan D. Majer
Received31 May 2011
Revised11 Aug 2011
Accepted16 Aug 2011
Published10 Dec 2011

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 [13]. 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 [46].

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., [1619]) and is becoming a major focus of myrmecological research worldwide (e.g., [2025]).

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.


DisturbanceAimIndicationEnvironmental parametersEffects on ant communityIndicator typeReference

AgricultureEvaluate the effect of different soil tillage and crop management systems on soil fauna groupsYes (implicit)Soil tillage and crop management systemsChange in species dominance (discriminant and correspondence analysis)EnvironmentalBaretta et al. [28]

AgricultureEvaluate the ant diversity in fig crops under different managementsYesTypes of soil cover plantsChange in density of species (, Tukey test)EnvironmentalMerlim et al. [29]

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

Agriculture (preceded by deforestation and fire)Assess the recolonization by fauna in areas cleared and burned to plant corn and beansYesHuman land-use and resting timeIncrease in abundance in the less-disturbed areas (non-statistical test)EnvironmentalNunes et al. [31]

Agriculture (formicid granulated baits)Evaluate the effect of different applications of formicide baits on nontarget ant communityYesForms and timing of application of formicid-granulated baitsNo effect of bait type on ant species richness (, ANOVA) Reduction in species richness observed only in control method, systematic application being more harmful (, ANOVA)EnvironmentalRamos et al. [32]

Anthropogenic activitiesQuantify heavy metals in worker ants of Camponotus rufipes collected in different environmentsYesObserved human interferenceThree groups of ants with different heavy metal concentrations (PCA analyses)EnvironmentalSilva et al. [33]

Conservation statusCreate an inventory of epigaeic ant species that occur in vine forest and use them to indicate the level of conservation of this ecosystemYesNoneInventory (nonstatistical test)Carvalho et al. [34]

Conservation statusVerify the impact of human use in mangrovesPotentialObserved levels of human useReduction on species richness EnvironmentalDelabie et al. [35]

Conservation statusInventory the ant community in the Baturité hillsYesNoneInventory (nonstatistical test)*Hites et al. [36]

Conservation statusStudy the ant communities in preserved and impacted savanna sitesYesObserved human interferenceReduction of diversity in impacted sites *EnvironmentalRamos et al. [37]

FireTest the negative effect of fire in Restinga environments on the ant communityPotentialPresence of fireIncrease in species richness with presence of fire (mean and confidence intervals of estimated species richness)EnvironmentalEndringer et al. [38]

FireTest the hypothesis that ant species richness and composition change after burning sand dunesYesHistory of fireMore ant species and distinct species composition in the unburned area (non-statistical test)EnvironmentalTeixeira et al. [39]

FragmentationVerify the responses of ants nesting in twigs in the litter layer to habitat changes associated with forest fragmentationPotentialDistance 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 edgeEcologicalCarvalho and Vasconcelos [40]

FragmentationDetermine the effect of forest fragmentation on ant communitiesYesRemnant 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 EcologicalGomes et al. [41]

FragmentationKnow the community of ants in forest fragmentsYesRemnant areaNo change in species richness with remnant area *EnvironmentalSantos et al. [42]

Forestry systemsDescribe the epigaeic ant communities in Eucalyptus plantationsYesEucalyptus ageNo change in species richness with Eucalyptus age EnvironmentalFonseca and Diehl [43]

Human land-useCompare the ant community structure between a crop and a secondary forestPotentialLand useReduction of diversity and equitability and change in species composition (non-statistical test)EnvironmentalCastro and Queiroz [44]

Human land-useCompare the impact of different agroecosystems on ant species richnessYesLand useHigher species richness in forest edges and pasture (non-statistical test); coffee crop presented reduced estimated richness EnvironmentalDias et al. [45]

Human land-useSurvey of ant and termite fauna in four patches with different vegetation structures and in one open fieldPotentialLand useChange in species richness and composition (non-statistical test)EnvironmentalDiehl et al. [46]

Human land-useTest the effects of Restinga soil characteristics on ant communitiesYes (implicit)Land use, physical and chemical soil properties, and microbial activityChange in species richness (non-statistical test) and composition (canonical correspondence analysis)EcologicalGomes et al. [47]

Human land-useElucidate ant species richness and community structure associated with the micro basin of Sanga Caramuru-ChapecóYesHabitat type, temperature, and rainfallChange 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)*EnvironmentalIlha et al. [48]

Human land-useDetermine the level of similarity of ant communities in forest areas (three native forest remnants) and an Eucalyptus reforestationYesLand useChange in species composition (Jaccard index— among Eucalyptus crops versus forest remnants and among forest remnants)EnvironmentalLapola and Fowler [49]

Human land-useTo inventory the ant fauna in a Cerrado area and in Eucalyptus plantations with five classes of understory agesYesEucalypt ageHigher density of species in Cerrado areas than in Eucalyptus (non-statistical test) and estimated species richness similar between areas EnvironmentalMarinho et al. [50]

Human land-useInvestigate the effect of structural characteristics of the environment on ant communitiesYesHabitat typeChange in species richness and composition (non-statistical test)EnvironmentalSantana-Reis and Santos [51]

Human land-useTest the hypotheses that there was a decrease in ant species richness and a change in the species composition in habitats with more intense soil useYesLand useSites with distinct soil use host a differential ant species composition (cluster analysis-Euclidean distance)EnvironmentalSchmidt and Diehl [52]

Human land-useEvaluate the effect of collection time (day and night) on ant fauna attracted to baits in areas of Eucalyptus cloeziana (Myrtaceae) and Cerrado (savanna vegetation)PotentialLand useCollection time effect was more important to ant fauna structure than the vegetation effect (ordination analyses)EnvironmentalTavares et al. [53]

Human land-use and successionCompare ant diversity under different land-use systemsYesLand use and age of successionChange in density of species (non-statistical test), species richness (sample-based accumulation curves and χ2), and composition (cluster analysis)*EnvironmentalBraga et al. [54]

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

LoggingTest the hypothesis that logging affects forest ant fauna by reducing the species richness and changing the composition of ground-foraging ant communitiesYesCanopy openness, abundance of understory vegetation, and leaf-litter depthChange 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 EcologicalKalif et al. [56]

MiningDetermine the levels of heavy metals in plants and identify soil organisms of the mesofauna that could be biological indicators of soil qualityYesPhysical and chemical soil properties and heavy metal contentDecrease in abundance and increase in lead (Pb) accumulation (non-statistical test)EnvironmentalBarros et al. [57]

MiningAnt fauna survey and community structure, analyses of the ground-dwelling ants in native vegetation and areas with different inferred copper levelsYesAreas with different inferred copper levelsDecrease in species richness with inferred copper levels (non-statistical test)EnvironmentalDiehl et al. [58]

Restoration (agriculture)Investigate the recolonization profile of the restored Atlantic ForestYesAge after plantingIncrease in species richness (, ANOVA) and change in species composition (ANOSIM, )*EnvironmentalPais and Varanda [59]

Restoration (anthropogenic disturbance)Test the hypothesis that ant fauna is closely related to the structural complexity of habitatYesAge of restorationChange in species composition (non-statistical test)EnvironmentalCoelho et al. [60]

Restoration (dredging disturbance)Evaluating ant bioindication of impacted habitatsYesTime since restoration, distance from the impact, and physical properties of soilChange 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)EnvironmentalCosta 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 AustraliaYesAge 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)EcologicalMajer [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 zonesYesAge 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)EcologicalMajer [63]

Restoration (mining)Investigate the community structure changes of different rehabilitation techniquesYesRehabilitation techniqueChange in species richness (non-statistical test) and composition (cluster analysis)EcologicalPereira et al. [64]

RoadTest 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 selectionPotentialPresence of dirt roadsThe number of colonization attempts in roads was 5 to 10 times greater than that in the adjacent vegetation EnvironmentalVasconcelos et al. [65]

SeasonalityInvestigate ant diversity and species composition on an islandYesSeasonalityChange in species richness and composition with seasonality (non-statistical test)*EnvironmentalSchmidt et al. [66]

SuccessionExamine whether secondary forests of the Brazilian Atlantic Forest act as refugia for forest-adapted speciesYes (implicit)Age of succession and soil typeRichness and composition of ant assemblages in secondary forests have recovered slowly and have not approached conditions typical to old-growth forestsEnvironmentalBihn et al. [67]

SuccessionExamine bait preferences of litter ants along a successional gradient of forestPotentialAge of successionPreference 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 antsEnvironmentalBihn et al. [68]

SuccessionInvestigate how functional diversity profile changed in a successional gradientPotentialAge of successionIncreased diversity and change in functional groups (non-statistical test)EnvironmentalBihn et al. [69]

SuccessionVerify patterns in the structure of ant communities along a successional gradientPotentialAge of successionIncreased diversity and equitability (non-statistical test)EnvironmentalCastro et al. [70]

SuccessionCompare ant diversity among sites in different successional stagesPotentialAge of successionHigher diversity in intermediary stage and change in composition (non-statistical test)EnvironmentalLeal et al. [71]

SuccessionCompare the diversity and composition of tree-dwelling ants in different successional stages of a seasonal deciduous forestPotentialAge of successionIncrease in species abundance and change in species composition (PCA analysis)EnvironmentalNeves et al. [72]

SuccessionCompare the ant species diversity related to successional stage and seasonalityYesAge of succession, tree richness and densityChange in species composition (DCA deterrent correspondence analysis, )EcologicalNeves et al. [73]

SuccessionEvaluate the long-term effect of fire on ant species richnessPotentialPresence of fire 15 years beforeChange in species composition (cluster analyses-Euclidean distance)EnvironmentalSantos et al. [74]

SuccessionAssess the changes in species richness and composition between relatively pristine habitat and along a forest regeneration gradientYesAge of successionIncrease in species richness (sample-based accumulation curves) and distinct species composition between pristine area and areas at regeneration (ANOSIM, *EnvironmentalSilva et al. [75]

SuccessionCompare the structure of the ground ant communities in areas at different levels of restorationYesAge of successionIncrease in species richness and decrease in abundance , change in species composition (ordination analysis)EnvironmentalVasconcelos [76]

SuccessionDetermine experimentally the effects of selective logging on ground-living antsYesLogging age, canopy cover, litter depth, and understory densitySpecies 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 plotsEcologicalVasconcelos et al. [77]

UrbanizationCompare the thermal tolerances of leaf-cutter ants (Atta sexdens) from colonies inside and outside an urban areaPotentialTemperatureUrban ants support higher temperatures better than rural ones, which present higher rates of mortality EnvironmentalAngilletta et al. [78]

Vegetation typeInventory antsYesHabitat typeChange in species richness (non-statistical test)*EnvironmentalDiehl et al. [79]

Vegetation typeTest how the diversity of one taxa can be a good surrogate of all diversityYesHabitat typeCorrelation with other taxa (Pearson correlation coefficients)BiodiversityLeal et al. [80]

Vegetation typeCompare ant diversity in three different forest stages (primary, reforestation, and secondary)PotentialHabitat typeChange in diversity and exclusive species (non-statistical test)*EnvironmentalLopes et al. [81]

Vegetation typeCompare 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 habitatsPotentialHabitat typeForests 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)EnvironmentalVasconcelos 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).

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.

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).


Ant speciesParameterHabitatReference

Acanthognathus brevicornisFrequency of occurrenceSecondary forest and area at early successionSilva et al. [75]
Acanthognathus ocellatus Frequency of occurrencePrimary forestSilva et al. [75]
Acanthognathus rudisFrequency of occurrencePrimary forestSilva et al. [75]
Acanthoponera mucronataFrequency of occurrenceNative forest remnantIlha et al. [48]

Acromyrmex balzaniPresence/absenceEucalyptus forestryMarinho et al. [50]
Presence/absenceLow human land-use-impacted sitesDelabie et al. [35]
Presence/absenceUndisturbed sites—control siteDiehl et al. [58]

Acromyrmex coronatusFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Frequency of occurrencePreserved savannaRamos et al. [37]

Acromyrmex lobicornisPresence/absenceUndisturbed sites—control siteDiehl et al. [58]
Acromyrmex lundiFrequency of occurrenceSecondary forestSchmidt and Diehl [52]
Acromyrmex niger Presence/absenceEucalyptus forestryMarinho et al. [50]
Acromyrmex rugosusFrequency of occurrenceTurnera ulmifolia fieldSantana-Reis and Santos [51]
Acromyrmex striatusPresence/absenceUndisturbed sites—control siteDiehl et al. [58]
Acromyrmex subterraneusFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Acromyrmex subterraneus brunneusPresence/absenceEucalyptus forestryMarinho et al. [50]
Acromyrmex subterraneus subterraneusPresence/absenceEucalyptus forestryMarinho et al. [50]
Acropyga decedensFrequency of occurrencePastureDias et al. [45]

Amblyopone armigeraFrequency of occurrencePreserved savannaRamos et al. [37]
Presence/absenceSavanna—cerrado sensu strictoMarinho et al. [50]
Frequency of occurrenceSecondary forest and area at early successionSilva et al. [75]

Amblyopone elongata Frequency of occurrencePrimary forestSilva et al. [75]
Anochetus diegensisFrequency of occurrencePreserved savannaRamos et al. [37]
Anochetus mayriFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Anochetus neglectusFrequency of occurrencePastureDias et al. [45]
Anochetus targioniiFrequency of occurrencePastureDias et al. [45]
Apterostigma acreFrequency of occurrenceForest fragmentDias et al. [45]
Apterostigma bolivianum Frequency of occurrenceForest fragmentDias et al. [45]
Atta robustaFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]

Atta sexdens rubropilosaPresence/absenceArea at early successionCoelho et al. [60]
Frequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Azteca alfariPresence/absenceArea at late succession stage—dry seasonNeves et al. [73]
Azteca muelleriFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Basiceros discigerFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Blepharidatta brasiliensisFrequency of occurrenceArea at late succession stageVasconcelos [76]
Brachymyrmex coactusFrequency of occurrenceSecondary forest and area at early successionSilva et al. [75]
Camponotus arboreusFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Camponotus atricepsPresence/absenceReforestated area at intermediate succession stageCoelho et al. [60]
Camponotus bidensPresence/absenceLow human land-use-impacted sitesDelabie et al. [67
Camponotus burtoniPresence/absenceEucalyptus forestryMarinho et al. [50]
Camponotus claviscapusPresence/absenceUndisturbed sitesDelabie et al. [35]

Camponotus crassusPresence/absenceBurned restingaEndringer et al. [38]
Frequency of occurrenceBurnt siteTeixeira et al. [39]
Frequency of occurrenceDisturbed sitesDiehl et al. [58]
Frequency of occurrenceSecondary forest and forest edgeLeal et al. [71]
IndValSavanna—vegetation and ground stratumVasconcelos and Vilhena [82]

Camponotus  fastigatusFrequency of occurrencePreserved savannaRamos et al. [37]

Camponotus  latangulusFrequency of occurrencePreserved savannaRamos et al. [37]
Presence/absenceSavanna—cerrado sensu strictoMarinho et al. [50]

Camponotus leydigiFrequency of occurrenceArea at early successionVasconcelos [76]

Camponotus melanoticusPresence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrencePastureDias et al. [45]
Presence/absenceArea at early successionCoelho et al. [60]

Camponotus novogranadensisFrequency of occurrenceArea at early successionVasconcelos [76]
Presence/absenceEucalyptus forestryMarinho et al. [50]
IndValForest—vegetation and ground stratumVasconcelos and Vilhena [82]
Frequency of occurrenceDisturbed savannaRamos et al. [37]

Camponotus punctatus minutiorFrequency of occurrencePreserved savannaRamos et al. [37]
Camponotus renggeriPresence/absenceEucalyptus forestryMarinho et al. [50]

Camponotus rufipesFrequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceForest fragmentsLapola and Fowler [49]

Camponotus sericeiventrisFrequency of occurrenceNative forest remnantIlha et al. [48]

Camponotus trapezoideusFrequency of occurrenceBurnt siteTeixeira et al. [39]
Frequency of occurrenceForest fragmentDias et al. [45]
Frequency of occurrencePreserved savannaRamos et al. [37]

Camponotus  vitatusPresence/absenceLow human land-use-impacted sitesDelabie et al. [35]
Camponotus westermanniPresence/absenceStrong human land-used-impacted sitesDelabie et al. [35]
Cardiocondyla obscuriorPresence/absenceArea at intermediate successionCoelho et al. [60]
Carebara urichiFrequency of occurrencePreserved savannaRamos et al. [37]

Cephalotes  atratusFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
IndValForest—vegetation stratumVasconcelos and Vilhena [82]

Cephalotes grandinosusPresence/absenceForestLopes et al. [81]

Cephalotes minutusPresence/absenceArea at early succession—dry seasonNeves et al. [73]
Presence/absenceLow human land-use-impacted sitesDelabie et al. [35]

Cephalotes pallidicephalusPresence/absenceLow human land-use-impacted sitesDelabie et al. [35]
Cephalotes pavoniiFrequency of occurrenceBurnt siteTeixeira et al. [39]
Cephalotes pellansPresence/absenceArea at intermediate succession—wet seasonNeves et al. [73]
Cephalotes pusillusIndValSavanna—vegetation and ground stratumVasconcelos and Vilhena [82]
Cephalotes simillimusIndValSavanna—vegetation stratumVasconcelos and Vilhena [82]
Crematogaster brasiliensisIndValForest—vegetation and ground stratumVasconcelos and Vilhena [82]

Crematogaster erectaPresence/absenceArea at intermediate successionCoelho et al. [60]
IndValSavanna—vegetation and ground stratumVasconcelos and Vilhena [82]

Crematogaster limataIndValForest—vegetation and ground stratumVasconcelos and Vilhena [82]
Crematogaster minutissimaIndValForest—ground stratumVasconcelos and Vilhena [82]
Crematogaster nigropilosaFrequency of occurrenceNative forest remnantIlha et al. [48]
Crematogaster quadriformisIndValSavanna—ground stratumVasconcelos and Vilhena [82]

Cyphomyrmex laevigatusFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Cyphomyrmex majorFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Cyphomyrmex olitorFrequency of occurrencePrimary forestSilva et al. [75]

Cyphomyrmex peltatusFrequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceForest fragmentsDias et al. [45]

Cyphomyrmex plaumanniFrequency of occurrencePrimary forestSilva et al. [75]

Cyphomyrmex salviniFrequency of occurrenceArea at early successionVasconcelos [76]
Frequency of occurrenceControl site (nonburnt)Teixeira et al. [39]

Cyphomyrmex transversusFrequency of occurrencePreserved savannaRamos et al. [37]

Discothyrea sexarticulataFrequency of occurrenceForest fragmentDias et al. [45]
Frequency of occurrencePrimary forestSilva et al. [75]

Dolichoderus attelaboidesIndValForest—vegetation stratumVasconcelos and Vilhena [82]
Dolichoderus bispinosusIndValForest—vegetation stratumVasconcelos and Vilhena [82]
Dolichoderus schulziPresence/absenceUndisturbed sitesDelabie et al. [35]
Dolichoderus voraginosusPresence/absenceArea at early succession—dry seasonNeves et al. [73]
Dorymyrmex guianensisIndValSavanna—ground stratumVasconcelos and Vilhena [82]

Dorymyrmex pyramicusFrequency of occurrenceBurnt siteTeixeira et al. [39]
Presence/absenceUndisturbed sitesDelabie et al. [35]

Dorymyrmex thoracicusIndValSavanna—ground stratumVasconcelos and Vilhena [82]
Eciton quadriglumeFrequency of occurrenceForest fragmentsLapola and Fowler [49]

Ectatomma brunneumPresence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceArea at early successionBraga et al. [54]
Presence/absenceLow human land-use-impacted sitesDelabie et al. [35]

Ectatomma edentatumFrequency of occurrencePreserved savannaRamos et al. [37]

Ectatomma lugensFrequency of occurrenceArea at late succession stageVasconcelos [76]
IndValForest—ground stratumVasconcelos and Vilhena [82]

Ectatomma muticumFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Ectatomma opaciventreIndValSavanna—ground stratumVasconcelos and Vilhena [82]

Ectatomma permagnumFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Frequency of occurrenceEucalyptus forestryBraga et al. [54]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Ectatomma planidensFrequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Ectatomma quadridensFrequency of occurrenceArea at early successionVasconcelos [76]

Ectatomma tuberculatumFrequency of occurrenceArea at early successionSilva et al. [75]
Presence/absenceBurned restingaEndringer et al. [38]
Presence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceArea at late succession stageBraga et al. [54]
Frequency of occurrenceSecondary forest and forest edgeLeal et al. [71]

Forelius maranhoensisIndValSavanna—ground stratumVasconcelos and Vilhena [82]
Gnamptogenys acuminataFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Gnamptogenys continuaFrequency of occurrencePrimary forestSilva et al. [75]
Gnamptogenys horniFrequency of occurrenceArea at late succession stageVasconcelos [76]
Gnamptogenys mediatrixFrequency of occurrenceForest fragmentDias et al. [45]

Gnamptogenys moelleriFrequency of occurrencePastureDias et al. [45]
Frequency of occurrenceSecondary forest and area at early successionSchmidt and Diehl [52]

Gnamptogenys reichenspergeriFrequency of occurrencePrimary forestSilva et al. [75]

Gnamptogenys striatulaPresence/absenceEucalyptus forestryMarinho et al. [50]
IndValForest—ground stratumVasconcelos and Vilhena [82]

Gnamptogenys sulcataPresence/absenceArea at early succession—wet seasonNeves et al. [73]
Gnamptogenys tortuolosaFrequency of occurrenceIntermediate disturbed areaVasconcelos [76]
Heteroponera flavaFrequency of occurrenceForest fragmentDias et al. [45]
Heteroponera micropsFrequency of occurrenceDisturbed habitat (Eucalyptus)Ilha et al. [48]
Hylomyrma balzaniFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Hylomyrma reitteriFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Hypoponera foedaFrequency of occurrenceNative forest remnantIlha et al. [48]
Hypoponera foreliFrequency of occurrencePreserved savannaRamos et al. [37]
Hypoponera opaciorFrequency of occurrenceDisturbed habitat (Eucalyptus)Ilha et al. [48]

Labidus coecusFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Presence/absenceUndisturbed sitesDelabie et al. [35]

Labidus praedatorFrequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceSecondary forestSchmidt and Diehl [52]

Leptogenys pusillaFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Leptothorax asperPresence/absenceEucalyptus forestryMarinho et al. [50]
Leptothorax spininodisPresence/absenceEucalyptus forestryMarinho et al. [50]

Linepithema humileFrequency of occurrenceBurnt siteTeixeira et al. [39]
Frequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]
Frequency of occurrenceForest fragmentsLapola and Fowler [49]

Megalomyrmex goeldiiFrequency of occurrenceArea at early successionSilva et al. [75]
Mycetagroicus cerradensisFrequency of occurrenceDisturbed savannaRamos et al. [37]
Mycetarotes paralelusPresence/absenceArea revegetated with native speciesPereira et al. [64]
Mycetophylax conformisPresence/absenceStrong human land-used-impacted sitesDelabie et al. [35]
Myrmicocrypta foreliFrequency of occurrencePreserved savannaRamos et al. [37]
Neivamyrmex orthonotusPresence/absenceEucalyptus forestryMarinho et al. [50]
Nesomyrmex spininodisPresence/absenceStrong human land-used-impacted sitesDelabie et al. [35]
Octostruma balzaniFrequency of occurrenceArea at intermediate successionBraga et al. [54]

Octostruma jheringhiFrequency of occurrenceForest fragmentDias et al. [45]
Frequency of occurrencePreserved savannaRamos et al. [37]

Odontomachus affinisFrequency of occurrenceSecondary forestSilva et al. [75]
Odontomachus bauriPresence/absenceEucalyptus forestryMarinho et al. [50]
Odontomachus brunneusFrequency of occurrencePreserved savannaRamos et al. [37]
Odontomachus caelatusFrequency of occurrenceArea at late succession stageVasconcelos [76]

Odontomachus cheliferFrequency of occurrencePastureBraga et al. [54]
Frequency of occurrencePreserved savannaRamos et al. [37]
Frequency of occurrenceSecondary forest and area at early successionSchmidt and Diehl [52]
Frequency of occurrenceSecondary forest and area at early successionSilva et al. [75]

Odontomachus haematodusFrequency of occurrenceArea at intermediate successionBraga et al. [54]
Presence/absenceBurned restingaEndringer et al. [38]
Frequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
IndValForest—ground stratumVasconcelos and Vilhena [82]

Odontomachus meinertiFrequency of occurrenceDisturbed savannaRamos et al. [37]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Oxyepoecus plaumanni Frequency of occurrencePrimary forestSilva et al. [75]
Oxyepoecus rastratusFrequency of occurrencePrimary forestSilva et al. [75]
Pachycondyla apicalis Presence/absenceEucalyptus forestryMarinho et al. [50]

Pachycondyla arhuacaFrequency of occurrenceArea at late succession stageBraga et al. [54]
Presence/absencePrimary restingaEndringer et al. [38]

Pachycondyla buckiFrequency of occurrencePrimary forestSilva et al. [75]
Pachycondyla crassinodaIndValForest—ground stratumVasconcelos and Vilhena [82]
Pachycondyla ferrugineaFrequency of occurrenceSecondary forest and area at early successionSilva et al. [75]
Pachycondyla gilberti Presence/absenceEucalyptus forestryMarinho et al. [50]

Pachycondyla harpaxPresence/absenceEucalyptus forestryMarinho et al. [50]
IndValForest—ground stratumVasconcelos and Vilhena [82]
Presence/absenceLow human land-use-impacted sitesDelabie et al. [35]

Pachycondyla obscuricornisFrequency of occurrenceEucalyptus (reforestation)Lapola and Fowler [49]

Pachycondyla stigmaFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Frequency of occurrencePrimary forestBraga et al. [54]

Pachycondyla striataFrequency of occurrencePreserved savannaRamos et al. [37]
Presence/absenceSavanna—cerrado sensu strictoMarinho et al. [50]
Frequency of occurrenceSecondary forest and area at early successionSchmidt and Diehl [52]
Frequency of occurrenceSecondary forest and area at early successionSilva et al. [75]

Pachycondyla villosaPresence/absenceBurned restingaEndringer et al. [38]
Frequency of occurrenceDisturbed savannaRamos et al. [37]

Paratrechina longicornisPresence/absenceEucalyptus forestryMarinho et al. [50]
Presence/absenceUndisturbed sitesDelabie et al. [35]

Pheidole diligensPresence/absenceArea at intermediate successionCoelho et al. [60]
Pheidole embolopyxFrequency of occurrenceArea at late succession stageVasconcelos [76]
Pheidole exiguaIndValForest—ground stratumVasconcelos and Vilhena [82]

Pheidole fimbriataFrequency of occurrencePreserved savannaRamos et al. [37]
Presence/absenceSavanna—cerrado sensu strictoMarinho et al. [50]

Pheidole fracticepsIndValForest—ground stratumVasconcelos and Vilhena [82]
Pheidole radoszkowskiiPresence/absenceLow human land-use-impacted sitesDelabie et al. [35]
Pheidole scalarisPresence/absenceArea at early succession—wet seasonNeves et al. [73]
Pogonomyrmex abdominalisPresence/absenceEucalyptus forestryMarinho et al. [50]
Pogonomyrmex naegeliiPresence/absenceArea at intermediate successionCoelho et al. [60]
Prionopelta punctulataFrequency of occurrenceSecondary forest and area at early successionSilva et al. [75]
Pseudomyrmex elongatusFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Pseudomyrmex filiformisFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Pseudomyrmex flavidulusIndValSavanna—vegetation stratumVasconcelos and Vilhena [82]

Pseudomyrmex gracilisPresence/absenceArea at intermediate successionCoelho et al. [60]
IndValSavanna—vegetation stratumVasconcelos and Vilhena [82]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Pseudomyrmex kuenckeliPresence/absenceUndisturbed sitesDelabie et al. [35]
Pseudomyrmex oculatusPresence/absenceArea at intermediate successionCoelho et al. [60]
Frequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Presence/absenceEucalyptus forestryMarinho et al. [50]
IndValForest—vegetation stratumVasconcelos and Vilhena [82]

Pseudomyrmex schuppiPresence/absenceArea at intermediate successionCoelho et al. [60]
Pseudomyrmex sericeusPresence/absenceUndisturbed sitesDelabie et al. [35]
Pseudomyrmex simplexPresence/absenceEucalyptus forestryMarinho et al. [50]
Pseudomyrmex spiculusPresence/absenceUndisturbed sitesDelabie et al. [35]

Pseudomyrmex tenuisFrequency of occurrenceArea at early successionVasconcelos [76]
IndValForest—vegetation and ground stratumVasconcelos and Vilhena [82]
Presence/absenceStrong human land-use-impacted sitesDelabie et al. [35]
Frequency of occurrenceArea at intermediate successionBraga et al. [54]
Frequency of occurrenceControl site (nonburnt)Teixeira et al. [39]

Pseudomyrmex termitariusPresence/absenceArea at early succession—dry seasonNeves et al. [73]
Frequency of occurrencePastureBraga et al. [54]
IndValSavanna—vegetation stratumVasconcelos and Vilhena [82]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Pyramica appretiataFrequency of occurrencePrimary forestSilva et al. [75]
Pyramica denticulataFrequency of occurrenceArea at early successionSilva et al. [75]
Pyramica lygatrix Frequency of occurrencePrimary forestSilva et al. [75]
Pyramica rugithoraxFrequency of occurrencePrimary forestSilva et al. [75]
Pyramica schulziPresence/absenceStrong human land-use-impacted sitesDelabie et al. [35]

Pyramica subdentataFrequency of occurrencePreserved savannaRamos et al. [37]
Frequency of occurrenceSecondary forest and area at early successionSilva et al. [75]

Pyramica zetekiFrequency of occurrencePreserved savannaRamos et al. [37]

Sericomymex bondariFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Presence/absenceLow human land-use-impacted sitesDelabie et al. [35]

Simopelta curvataFrequency of occurrencePasture (edge)Dias et al. [45]

Solenopsis geminataFrequency of occurrenceArea at early successionVasconcelos [76]
Frequency of occurrenceCaesalpinia echinata forestSantana-Reis and Santos [51]

Solenopsis saevissimaFrequency of occurrenceDisturbed sitesIlha et al. [48]
Presence/absenceEucalyptus forestryMarinho et al. [50]

Solenopsis substitutaFrequency of occurrenceBurnt siteTeixeira et al. [39]
Presence/absenceEucalyptus forestryMarinho et al. [50]
IndValSavanna—ground stratumVasconcelos and Vilhena [82]

Sphinctomyrmex staliFrequency of occurrencePrimary forestSilva et al. [75]
Stegomyrmex vizzotoi Frequency of occurrencePrimary forestSilva et al. [75]
Strumigenys denticulataFrequency of occurrenceIntermediate disturbed areaVasconcelos [76]

Strumigenys elongataFrequency of occurrenceArea at early successionSilva et al. [75]
Frequency of occurrencePreserved savannaRamos et al. [37]

Strumigenys perparvaPresence/absenceSavanna—cerrado sensu strictoMarinho et al. [50]
Frequency of occurrencePreserved savannaRamos et al. [37]

Tapinoma melanocephalumFrequency of occurrenceDisturbed habitat (Eucalyptus)Ilha et al. [48]
Frequency of occurrenceForest fragmentsLapola and Fowler [49]

Trachymyrmex cornetziFrequency of occurrenceControl site (nonburnt)Teixeira et al. [39]
Trachymyrmex fuscusFrequency of occurrencePasture (edge)Dias et al. [45]
Trachymyrmex zetekiFrequency of occurrencePrimary forestSilva et al. [75]

Typhlomyrmex majorFrequency of occurrenceForest fragmentsLapola and Fowler [49]
Frequency of occurrencePrimary forestSilva et al. [75]

Typhlomyrmex pusillusFrequency of occurrencePrimary forestSilva et al. [75]

Wasmannia auropunctataPresence/absenceArea at intermediate successionCoelho et al. [60]
Frequency of occurrenceControl site (nonburnt)Teixeira et al. [39]

Wasmannia rochaiPresence/absenceArea at early successionCoelho 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, 8991]; 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, 9699], 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., [100105]) 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, 106109]).

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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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.


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