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

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.