ARTIGO_Ants as indicators in Brazil...

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Volume 2012, Article ID 636749,23pages doi: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. Solar}

3

1_{Laboratory of Ant Ecology, Sector of Ecology, Department of Biology, Federal University of Lavras,}

37200-000 Lavras, MG, Brazil

2_{Institute of Education of Divinópolis, Educational Foundation of Divinópolis, 35501-170 Divinópolis, MG, Brazil}

3_{Post-Graduate Program in Entomology, Department of Entomology, Federal University of Vic¸osa,}

36570-000, Vic¸osa, MG, Brazil

Correspondence should be addressed to Carla R. Ribas,[email protected]

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. 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 moni-toring programs. By doing so, we expect to encourage new research on ants as bioindicators as well as to summarize current know-ledge, facilitating further research.

1. Introduction

Intensive exploitation of natural resources and the resulting impacts on pristine habitats have led to calls from the scien-tific community and the general public to measure or

moni-tor the level of these environmental impacts [1–3].

Bioindi-cators are a useful way to evaluate such impacts, since chang-es 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

bioin-dication into three categories according to the three main ap-plications: (i) environmental indicators: used to detect or monitor changes in the environmental state, (ii) ecological indicators: used to demonstrate the impact of an environ-mental stress on the biota or monitor longer-term stress-in-duced 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 indi-cator species must have, the most notable being ease of mea-surement, 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 rehabi-litation 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

ecolog-ical studies [10,11]. This group has useful characteristics for

successful indication and monitoring of environmental im-pacts, 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 envi-ronmental 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

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a major focus of myrmecological research worldwide (e.g.,

[20–25]).

Although ants are a simple, cheap, and powerful indi-cator of environmental impacts and rehabilitation (e.g., in

Australia [17]), in Brazil, a country which harbours

enor-mous diversity and complexity of habitats, the standard use of ants as indicators is still relatively new and should be

eval-uated 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],

en-vironmental, ecological, or biodiversity indicators, we des-cribe 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, restrict-ing our search to those carried out in Brazil. To encompass a broad time range of papers, we used the following key-words in Portuguese and English, respectively: “formiga,” “ant,” “indicador,” “bioindicador,” “indicator,” “bioindica-tor,” “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 ob-served, the results which were obtained, and the main con-clusion reached in the study.

We define the paper as specifically analyzing ants as indi-cators 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 pa-pers.” 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 consid-ered 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, name-ly: habitats with agricultural activities only, habitats with nat-ural vegetation only, and habitats with both agricultnat-ural acti-vities and natural habitats. Similarly, “Succession” studies were those investigating natural succession, and

“Restora-tion” studies were those evaluating diﬀerent rehabilitation

techniques, such as succession following managed

restora-tion eﬀorts.

We used McGeoch [7] as a reference to decide if the ants

were used as environmental, ecological, or biodiversity

indi-cators in the reviewed papers (see McGeoch’s [7] definition

in the introduction section). Moreover, we defined ant spec-ies as indicators when there was a specspec-ies list in the paper showing the occurrence of ants in specific sites or when the author considered the ant species to be an indicator else-where 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 dis-turbance, summarizing responses, and relating the most fre-quent responses to the most frefre-quently used sampling meth-odologies 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

indi-cation paper” [83]. The others specifically mentioned the

in-tention 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 in-dicators but to suggest new tools to simplify their use as indicators.

From the 58 papers, exactly half (29) were published in English and the other half in Portuguese. Among the “Poten-tial 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 bio-indicators 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,

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Ta b le 1: P apers re vi ew ed re gar ding ants as indicat ors in B ra zil, indicating the m ain distur b anc e in ve stigat ed (Distur b anc e), the aim of the p aper (A im), if the paper w as ex plicitly ,i mplicitly o r has the P o te ntial to b e u sed in indicat or studies (I ndication), the en vi ro nmental p ar amet ers analyz ed/sampled (En vi ro nmental p ar amet ers), the re sponses o f ant co mm unit y to distur b anc e that w er e found to be sig nificant (E ff ects on ant comm unit y), the indicat or ty pe used (I ndicat or ty pe) and the p aper (R efer enc e). Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e A gr icultur e Ev al u at e th e eff ect o f d iff er ent soil tillage and cr o p management syst ems o n soil fauna gr oups Y es (implicit) Soil tillage and cr o p management syst ems Change in species d ominanc e (discr iminant and cor re sp ondenc e analysis) En vi ro nmental B ar etta et al. [ 28 ] A gr icultur e E val uat e the ant di ve rsit y in fi g cr o p s under di ff er ent managements Y es T yp es of soil co ve r p lants Change in densit y o f species (P< 0. 05, Tu ke y te st ) En vi ro nmental M erlim et al. [ 29 ] A gr icultur e (for est ry pr ac ti ce s in Eu ca ly p tu s) U se the ant guild conc ept to ev aluat e ch anges in Eu ca ly p tu s plantations follo w ing co nt ro l o f leaf-cutting ants Y es F or est ry p ra ctic es Change in species composition—obser ve d fr equency o f species and guilds (non-statistical te st) En vi ro nmental L acau et al. [ 30 ] A gr icultur e (pr ec eded b y defor estation and fi re ) A ssess the rec olonization b y fauna in ar eas cl ear ed and b ur ned to plant cor n and beans Ye s H u man land-use and re sting time In cr ease in abundanc e in the less-distur b ed ar eas (non-statistical te st) En vi ro nmental N unes et al. [ 31 ] A gr icultur e (for micid gr an ulat ed baits) Ev al u at e th e eff ect o f d iff er ent applications of for m icide b aits on nontarget ant co mm unit y Ye s F o rm s and timing of application o f for m icid-g ran ulat ed baits No eff ect o f b ait ty p e o n ant species ric hness (P> 0. 05, ANO V A) R eduction in species ri chness obser ved only in co nt ro l m ethod, syst ematic application b eing mor e har mful (P< 0. 05, ANO V A) En vi ro nmental R amos et al. [ 32 ] A n thr o pogenic acti vi ties Quantify hea vy m etals in w or ke r ants of Camponotus ru fipes co ll ec te d in d iff er ent en vi ro nments Ye s Ob se rv ed h u m an int er fer enc e Thr ee gr o ups of ants w ith di ff er ent h ea vy metal conc ent ra tions (PCA analyses) En vi ro nmental Sil va et al. [ 33 ] Con ser va ti on status C reat e an in vent o ry of epigaeic ant species that o cc ur in vine for est and u se them to indicat e the le ve l of co nser vat ion of this ec osyst em Y es N one In vent o ry (nonstatistical test) — C ar valho et al. [ 34 ] Con ser va ti on status V er ify the impact o f h uman use in mang ro ve s P o te ntial O b ser ved le ve ls of h u man use R eduction o n species ri chness (R 2= 0. 53, P = 0. 007) En vi ro nmental D elabie et al. [ 35 ] Con ser va ti on status In ve nt or y the ant comm unit y in the B atur it é hills Y es N one In vent o ry (nonstat ist ical test) ∗ — H it es et al. [ 36 ] Con ser va ti on status Stud y the ant comm unities in pr eser ve d and impact ed sa vanna sit es Ye s Ob se rv ed h u m an int er fer enc e R eduction o f d iv ersit y in impact ed sit es (F = 101 .62, P< 0. 0001) ∗ En vi ro nmental R amos et al. [ 37 ] Fir e Te st th e n eg at iv e eff ect o f fi re in Re st in ga en vi ro nments on the ant co mm unit y P o te ntial P re senc e o f fi re In cr ease in sp ecies ri chness w ith pr esenc e of fir e (mean and confidenc e int er vals of estimat ed sp ecies ri chness) En vi ro nmental E ndr inger et al. [ 38 ]

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Ta b le 1: C o ntin ued. Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e Fir e T est the h yp othesis that ant species ri chness and composition ch ange aft er b ur ning sand dunes Y es H ist o ry of fir e M o re ant sp ecies and distinct sp ecies co mposition in the unbur ned ar ea (non-statistical te st) En vi ro nmental T eix eir a et al. [ 39 ] F rag mentation V er ify the responses of ants nesting in tw ig s in the litt er la ye r to habitat changes associat ed w ith for est fr ag mentation P o te ntial Distanc e to for est edge, re mnant isolation, leaf-litt er d epth, d ensit y of dead tw ig s, and vegetation (thr ee par amet ers measur ed) H ig h er species ric hness (F = 8. 56, P = 0. 006); m ost ant sp ecies h ad gr eat er nest densities in contin u ous ar eas than in re mnants, change in species co mposition (F = 8. 14, P = 0. 001) w ith for est edge Ec olog ical Car valho and V asc onc elos [ 40 ] F rag mentation Det er m ine the eff ect o f for est fr ag mentation o n ant co mm unities Ye s R emnant ar ea, distanc e to for est edge, vegetation co ve r o f m at ri x, and ve ge ta ti o n (t h re e par amet ers measur ed) No eff ec to fm an yf ra gm en tc h ar ac te ri st ic s on ant sp ecies ri chness: ar ea (F = 8. 22, P = 0. 77), distanc e cor e-bor d er (F = 64 .86, P = 0. 42). O nly tr ee d ensit y had an eff ect (F = 46 .30, R 2= 23 .32, P = 0. 02) Ec olog ical G omes et al. [ 41 ] F rag mentation K n o w the comm unit y o f ants in for est fr ag ments Y es R emnant ar ea N o ch ange in species ric hness w ith re mnant ar ea (R 2= 0. 02, F = 0. 22, P = 0. 64) ∗ En vi ro nmental S ant o s et al. [ 42 ] F o re st ry syst ems Descr ibe the epigaeic ant co mm unities in Eu ca ly p tu s plantations Ye s Eu ca ly p tu s age N o ch ange in species ric hness w ith Eu ca ly p tu s age (P = 0. 58) En vi ro nmental F onseca and D iehl [ 43 ] Hu m an land-use C o mpar e the ant comm unit y st ru ctur e b etw een a cr o p and a sec o ndar y for est P o te ntial L and u se R eduction o f d iv ersit y and equitabilit y and ch ange in species composition (non-statistical te st) En vi ro nmental Cast ro and Q ueir o z [ 44 ] Hu m an land-use C o mpar e the impact of di ff er ent ag ro ec osyst ems on ant sp ecies ri chness Ye s L an d u se H ig h er species ric hness in for est edges and pastur e (non-statistical test); co ff ee cr o p pr esent ed reduc ed estimat ed ric hness (h = 10 .85, P> 0. 05) En vi ro nmental D ias et al. [ 45 ] Hu m an land-use Su rv ey of ant and te rm it e fauna in four pat ches w ith d iff er ent ve getation st ru ctur es and in o ne op en fi eld P o te ntial L and u se Change in species ric hness and composition (non-statistical te st) En vi ro nmental D iehl et al. [ 46 ] Hu m an land-use Te st th e eff ects of Re st in ga soil ch ar act er istics o n ant co mm unities Y es (implicit) Land use, ph ysical and ch emical soil pr o p er ties, and m icr o bial acti vi ty Change in species ric hness (non-statistical te st) and co mposition (canonical co rr espondenc e analysis) Ec olog ical G omes et al. [ 47 ] Hu m an land-use El ucidat e ant species ri chness and co mm unit y st ructur e associat ed wi th th e m ic ro b as in o f S an ga Car am u ru -Chapec ó Ye s H abitat ty p e, te mp er atur e, and rainfal l Change in species composition (B ra y-C u rt is Cl ust er A nalysis indicat ed hig her similar it y for distur b ed ar eas) and hig her ric hness (obser ve d and estimat ed) in the n ati ve ar ea (sample-based ac cum ulation cur ve s) ∗ En vi ro nmental Ilha et al. [ 48 ]

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Ta b le 1: C o ntin ued. Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e Hu m an land-use Det er m ine the le vel of similar it y of ant comm unities in for est ar eas (thr ee nati ve for est re mnants) and an Eu ca ly p tu s re fo re st at io n Ye s L an d u se Change in species composition (J ac car d inde x— CJ = 0. 29 ± 0. 02 among Eu ca ly p tu s cr ops ve rs us fo re st re m n an ts an d CJ = 0. 40 ± 0. 06 among for est remnants) En vi ro nmental L apola and F o w ler [ 49 ] Hu m an land-use T o in ve nt or y the ant fauna in a Cer rad o ar ea and in Eu ca ly p tu s plantations w ith fi ve cl asses o f underst or y ages Ye s E u ca ly p t ag e H ig h er densit y o f species in Cer rad o ar eas than in Eu ca ly p tu s (non-statistical te st) and estimat ed sp ecies ri chness similar b etw een ar eas (h = 1. 6, P> 0. 05) En vi ro nmental M ar inho et al. [ 50 ] Hu m an land-use In ve stigat e the eff ec to fs tr u ct u ra l ch ar act er istics o f the en vi ro nment on ant comm unities Y es H abitat ty p e Change in species ric hness and composition (non-statistical te st) En vi ro nmental Santana-R eis and Sant os [ 51 ] Hu m an land-use T est the h yp otheses that ther e was a d ecr ease in ant species ric hness and a ch ange in the sp ecies co mposition in h abitats w ith m or e int ense soil use Ye s L an d u se Si te s w ith distinct soil u se host a d iff er ent ial ant species co mposition (c lust er analysis-E uc lidean distanc e) En vi ro nmental S ch midt and D iehl [ 52 ] Hu m an land-use Ev al u at e th e eff ect o f col lection time (da y and nig ht) o n ant fauna att ract ed to b aits in ar eas of E u caly ptus cloeziana (M yr tac eae) and C er ra d o (sa vanna ve getation) P o te ntial L and u se C o llectio n time eff ect w as mor e impor tant to ant fauna st ru ctur e than the ve getation eff ect (or dination analyses) En vi ro nmental T av ar es et al. [ 53 ] Hu m an land-use and su cce ss io n C o mpar e ant di ve rsit y under di ff er ent land-use syst ems Ye s Land use and age o f su cce ss io n Change in densit y o f sp ecies (non-statistical te st), species ric hness (sample-based ac cum u lation cur ves and χ2), and co mposition (c lust er analysis) ∗ En vi ro nmental B ra ga et al. [ 54 ] In undation Document the ant fauna in thr ee di ff er ent for est ty p es (one ann u ally in undat ed and tw o o n te rr a fi rm e) P o te ntial Ve ge ta ti o n (s ev er al par amet ers measur ed) Change in di ve rsit y, similar it y, and pr op or ti on of di ff er ent n esting and feeding habitats (non-statistical te st) Ec olog ical M ajer and D elabie [ 55 ] Logg ing T est the h yp othesis that logg ing aff ects for est ant fauna b y re ducing the species ri chness and chang ing the comp o sit ion of gr ound-for ag ing ant comm unities Ye s Cano p y o p enness, abundanc e o f underst or y ve getation, and leaf-litt er dep th Change in sp ecies comp o sit ion pr op or ti on of Ph ei d ol e was reduc ed fr om 21.4% and 26% in unlogged for est and lo w-impact logg ing ,r esp ecti vely ,t o 14.8% in hig h-impact logg ing (F = 4. 99, P< 0. 05) Ec olog ical K alif et al. [ 56 ]

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Ta b le 1: C o ntin ued. Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e M ining Det er m ine the le vels o f h ea vy metals in plants and identify soil org anisms of the m esofauna that co uld b e b iolog ical indicat ors o f soil qualit y Ye s Ph ysical and chemical soil pr op er ties and h ea vy metal co nt ent Decr ease in abundanc e and incr ease in lead (Pb) ac cum u lation (non-statistical te st) E n vi ro n m en ta l B ar ro s et al .[ 57 ] M ining A n t fauna sur ve y and comm unit y st ru ctur e, analyses of the gr ound-d w elling ants in nati ve ve getation and ar eas w ith di ff er ent infer re d co p per le vels Ye s A reas w ith di ff er ent infer re d co p per le vels Decr ease in species ri chness w ith infer re d co pp er le ve ls (non-statistical te st) En vi ro nmental D iehl et al. [ 58 ] R est or ation (ag ricultur e) In ve stigat e the re colonization pr ofile of the rest o re d A tlant ic Fo re st Y es A ge aft er p lanting In cr ease in sp ecies ri chness (P< 0. 05, ANO V A) and change in species co mposition (ANOSIM, P< 0. 01) ∗ En vi ro nmental P ais and V ar anda [ 59 ] R est or ation (anthr o p ogenic distur b anc e) T est the h yp othesis that ant fauna is closely relat ed to the str uctur al co mplexit y of habitat Y es A ge of re st or at ion Change in species composition (non-statistical te st) En vi ro nmental C oelho et al. [ 60 ] R est or ation (dr edg ing distur b anc e) E val uating ant b ioindication o f impact ed habitats Ye s T ime sinc e rest o ra tion, distanc e fr o m the impact, and p h ysical p ro per ties o f soil Change in species ric hness: hig her in ce rr ad o than in the re st or ation h abitats, and also hig her in the ec ot one and int er mediat e zo nes than o n the beac h (F = 3. 95, P< 0. 05) and change in abundanc e (F = 1. 9, P< 0. 046) and co mposition (non-statistical test) En vi ro nmental C osta et al. [ 61 ] R est or ation (mining) In ve stigat e w hic h ants rec oloniz ed re cl aimed ar eas in subt ro pical re gi ons and ev al uat e the eff ect o f di ff er ent rehabilitation tec hniques, co mpar ing re sults w ith A ust ralia Ye s A ge o f rehabilitation, soil penet rabilit y, n u mber of log s, litt er and ve getation measur es (thr ee and fi ve par amet er ,r esp .) In cr ease in sp ecies ri chness (non-statistical te st) and ch ange in co mposition (PC oA) Ec olog ical M ajer [ 62 ] R est or ation (mining) Ev al u at e th e effi cacy of re habilitation pr oc edur es in mining sit es o n facilitating ant re colonization and co mpar e it w ith other tr o pical re gi ons and cl imatic zo nes Ye s A ge o f rest o ra ti on, soil penet rabilit y, litt er depth, p er centage of litt er ,g ra ss, an dh er bc o ve r,a n d ve ge ta ti o n (s ev er al par amet ers measur ed) Species ric hness incr eased in early ages but slo w ed in lat e ages and w as smal ler than co nt ro l sit e (non-statistical te st). Distinct sp ecies composition in sit es at early ages, int er mediat e ages, and co nt ro l sit es (or dination analyses) Ec olog ical M ajer [ 63 ] R est or ation (mining) In ve stigat e the co mm unit y st ru ctur e changes of di ff er ent re habilitation te chniques Y es R ehabilitation tec hnique Change in species ric hness (non-statistical te st) and co mposition (c lust er analysis) Ec olog ical P er eir a et al. [ 64 ] Ro ad T est the h yp othesis that dir t roads ar e fa vo ur able landing sit es for A tta lae vigata founding queens. A n alyz e the impor tanc e of litt er co ve r as a pr o ximat e cue in nest-sit e selection P o te ntial P re senc e o f dir t roads The n umber o f colonization att empts in ro ads w as 5 to 1 0 times gr eat er than that in the adjac ent vegetation (P< 0. 001) En vi ro nmental V asc o nc elos et al. [ 65 ]

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Ta b le 1: C o ntin ued. Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e Seasonalit y In ve stigat e ant di ve rsit y and sp ecies comp o sit ion on an island Y es S easonalit y Change in species ric hness and composition w ith seasonalit y (non-statistical te st) ∗ En vi ro nmental S ch midt et al. [ 66 ] Su cce ss io n Examine whether sec ondar y for ests o f the B razilian A tlantic F o re st act as refug ia for for est-adapt ed species Y es (implicit) A ge o f suc ce ssion and soil ty p e Ric hness (P< 0. 001) and composition (P< 0. 004) of ant assemblages in sec ondar y for ests h av e rec o ver ed slo w ly and h av e n ot appr oac h ed co nditions ty pical to old-g ro w th for ests En vi ro nmental B ihn et al. [ 67 ] Su cce ss io n Examine bait pr efer enc es o f litt er ants along a suc ce ssional gr adient of for est P o te ntial A ge of suc ce ssion P refer enc e of ants for the ty p e of bait ch anged along the suc ce ssional gr adient (F = 5. 52, P = 0. 02). In young suc ce ssional stages, N baits att ra ct ed mor e ants than CHO b aits, w her eas in lat e suc ce ssional stages, C HO baits att ra ct ed mor e ants En vi ro nmental B ihn et al. [ 68 ] Su cce ss io n In ve stigat e h o w functional di ve rsit y p ro file changed in a suc ce ssional gr adient P o te ntial A ge of suc ce ssion In cr eased di ve rsit y and ch ange in functional gr oups (non-statistical te st) En vi ro nmental B ihn et al. [ 69 ] Su cce ss io n V er ify patt er ns in the st ructur e of ant comm unities along a suc ce ssional gr adient P o te ntial A ge of suc ce ssion In cr eased di ve rsit y and equitabilit y (non-statistical te st) En vi ro nmental C ast ro et al. [ 70 ] Su cce ss io n C o mpar e ant di ve rsit y among sit es in di ff er ent suc ce ssional stages P o te ntial A ge of suc ce ssion H ig h er di ve rsit y in int er mediar y stage and ch ange in co mposition (non-statistical test) En vi ro nmental L eal et al. [ 71 ] Su cce ss io n C o mpar e the di ve rsit y and co mposition o f tr ee-d w elling ants in di ff er ent suc ce ssional stages of a seasonal deciduous for est P o te ntial A ge of suc ce ssion In cr ease in species abundanc e (F = 9. 26, P = 0. 003) and change in species composition (PCA analysis) En vi ro nmental N ev es et al. [ 72 ] Su cce ss io n C o mpar e the ant species di ve rsit y re lat ed to suc ce ssional stage and seasonalit y Ye s A ge o f su cce ss io n ,t re e ri chness and d ensit y Change in species composition (D CA de te rr ent cor re sp ondenc e analysis, P< 0. 001) Ec olog ical N ev es et al. [ 73 ] Su cce ss io n E va lu ate th e lo n g-te rm eff ect o f fir e o n ant species ric hness P o te ntial P resenc e of fir e 1 5 years be fo re Change in species composition (c lu st er analyses-E uc lidean distanc e) En vi ro nmental S ant o s et al. [ 74 ] Su cce ss io n A ssess the changes in species ri chness and composition betw een re lati ve ly pr istine habitat and al o n g a fo re st re ge n er at io n gr adient Y es A ge of suc ce ssion In cr ease in sp ecies ri chness (sample-based ac cum u lation cur ves) and distinct species co mposition b etw een pr istine ar ea and ar eas at re gener ation (ANOSIM, R = 0. 79, P< 0. 001) ∗ En vi ro nmental Sil va et al. [ 75 ] Su cce ss io n C o mpar e the st ru ctur e o f the gr ound ant comm unities in ar eas at di ff er ent le ve ls o f rest o ra ti on Y es A ge of suc ce ssion In cr ease in sp ecies ri chness (F = 5. 1, P = 0. 01) and d ecr ease in abundanc e (F = 8. 1, P< 0. 001), change in species composition (or dination analysis) En vi ro nmental V asc o nc elos [ 76 ]

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Ta b le 1: C o ntin ued. Distur banc e A im Indication E n vir onmental par amet ers Eff ects on ant comm unit y Indicat or ty pe R efer enc e Su cce ss io n Det er m ine ex per imentally the eff ec ts of selec ti ve logg ing on gr ound-li ving ants Ye s Logg ing age, cano p y co ve r, litt er depth, and underst or y densit y Species ric hness, ev enness, and abundanc e per p lot did not var y among tr eat ments (P> 0. 05). M ost o f the species found in the co nt ro l p lots w er e also p re sent in the logged plots Ec olog ical V asc o nc elos et al. [ 77 ] U rbanization C o mpar e the ther mal toler anc es of le af -c u tt era n ts( A tta se xde n s) fr om colonies inside and outside an ur ban ar ea P o te ntial T emper atur e U rban ants suppor t hig her temper atur es bett er than ru ra l o nes, whic h p re sent hig her ra te s o f m o rt al ity (β = 20 .54 .237, P = 0. 02) En vi ro nmental A ng illetta et al. [ 78 ] V ege tat ion ty p e In ve nt or y ants Y es H abitat ty p e Change in species ric hness (non-statistical te st ) ∗ En vi ro nmental D iehl et al. [ 79 ] Ve ge ta ti o n ty p e T est ho w the di ve rsit y o f o ne taxa ca nb eag o o d su rr o ga teo fa ll di ve rsit y Y es H abitat ty p e C o rr elation w ith o ther taxa (P earson co rr el at io n co effi cients) B iodi versit y L eal et al. [ 80 ] Ve ge ta ti o n ty p e C o mpar e ant di ve rsit y in thr ee di ff er ent for est stages (pr imar y, re for estation, and sec ondar y) P o te ntial H abitat ty pe Change in di ve rsit y and ex cl usi ve species (non-statistical te st) ∗ En vi ro nmental Lop es et al. [ 81 ] Ve ge ta ti o n ty p e C o mpar e the ant fauna fr om for ests and near b y pat ches o f sa vanna (Cer ra d o ) in the B razilian A m az on. A ssess whether ther e is a di ff er enc e in the fauna betw een the gr o und and lo w er ve getation st ra ta in both habitats P o te ntial H abitat ty pe F o re sts h ost tw ic e as man y species as sa vanna (sample-based rar efaction cur ves). In both habitats, the gr ound host ed mor e species than vegetation (P< 0. 005). D istinct sp ecies comp o sit ion b etween for est and sa vanna and b etw een gr ound and vegetation w ithin the same h abitat; ant species fi delit y and specificit y is gi ven b y IndV al (see Ta b le 2 ) En vi ro nmental V asc onc elos and Vi lh en a [ 82 ] ∗ pap ers w ith sample-based ac cum ulation cur ves.

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Years of publication 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 N u mber of analyz ed papers 0 5 10 15 20 25 30 35 40 Indication papers Potential indication papers

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.

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 stud-ies).

The majority of studies sampled ants at the soil surface (44), but some studies also considered the soil surface to-gether 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

besid-es disturbance (Table 1).

The parameters of the ant faunas that were most com-monly related to the disturbance type were ant species rich-ness 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 param-eter was sensitive to disturbance, although if we considered only those papers with statistical analyses, the number dec-reases to 21. Summarizing the papers that analyze species richness or diversity, the responses found were species rich-ness 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 statisti-cally, 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

sensi-tive to disturbance in the majority of papers in which this parameter was tested, irrespective of the sampling method-ology, 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 pit-fall traps revealed a positive response of ant species richness or diversity to disturbance. Nevertheless, when we

consid-ered 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 eco-logical 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 fre-quency 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

speci-fic habitats (Table 2). The genera with higher numbers of

indicator species were Camponotus (18), Pseudomyrmex (12),

Pachycondyla (11), Ectatomma (9), Gnamptogenys (9), Acro-myrmex (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).

4. Discussion

It has been possible to determine the history of research car-ried 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 “In-dication papers” were published, which increased in the fol-lowing years and exceeded the “Potential indication papers” in 2001.

Regarding the idiom of the papers, it is interesting to ob-serve that half of the papers are still published in Portuguese. In spite of the growing internationalization of Brazilian

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Sampling methods

Baits Baits and

hand collecting

Multiple Pitfall Winkler

N umber of re sults 0 2 4 6 8 10 12 14 16 Composition changed Composition not changed

(a)

Sampling methods

Baits Baits and

hand collecting

Multiple Pitfall Winkler

N umber of re sults 0 2 4 6 8 10 12 14 16 S increased S not altered S decreased S changed (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. 0 1 2 3 4 5 6 Sampling methods

Baits Multiple Pitfall Winkler

N umber of re sults Composition changed Composition not changed

(a)

Sampling methods

Baits Multiple Pitfall Winkler

N u mb er of re sults S not altered S decreased S changed 0 1 2 3 4 5 6 7 (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.

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0 2 4 6 8 10 12 Sampling methods Multiple N u mb er of re sults Composition changed Composition not changed

Baits and hand collecting Baits (a) 0 2 4 6 8 10 12 Sampling methods Multiple N u mb er of re sults Baits and hand collecting Baits S decreased S changed (b)

Figure 4: Papers that analyzed (a) ant species composition and/or (b) ant species richness/diversity without statistical tests and their res-ponses 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 in-creased with disturbance. S not altered—species richness or diversity not aﬀected by disturbance. S dein-creased—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.

research [86,87], many Brazilian studies that use ants as

bio-indicators 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 im-proving 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 ex-change with researchers from other countries reinforces the maturation of this area of research. Examples include Brazil-ian scientists that complete their Ph.D. studies abroad the possibility for doctorate students to undertake international exchange programs, and the internationalization of the Bra-zilian Symposium of Myrmecology.

However, it is important to clarify that although some au-thors 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

pro-perly (i.e., sampling in just one habitat, without diﬀerent

levels of the disturbance/restoration and control sites) or be-cause 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 stratifi-cation, 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

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programs usually have short-term goals, it is desirable to balance the benefits and costs of using several types of sam-pling methods compared to using only one samsam-pling method

which could achieve similar reliable results (Figures 2(a)

and2(b)), compare multiple sampling and pitfall outcomes)

about the patterns and aims under investigation.

The most used sampling method in the studies was at-tractive baits, which are more suitable for behavioural

ques-tions [92] and are useful for verifying the presence and

popu-lation trends of invasive and keystone ant species [13].

How-ever, 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 do-minate 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 Figures3(a)and3(b),

which shows that the sole use of baits revealed apparently un-changing species composition and no trend in species

rich-ness. Thus, Underwood and Fisher [13] recommend the use

of pitfall traps and litter sampling (The Winkler and/or Ber-lese extractors) as eﬀective ant sampling methods for moni-toring goals related to the eﬀect of habitat disturbance and transformation on ant diversity, which is corroborated in

Figures3(a),3(b),4(a), and4(b).

Species richness and diversity and species composition are the parameters of ant communities most commonly ana-lyzed 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 Figures3and4). This coarse

re-lationship of species richness to disturbance is probably be-cause ants are generalists, so the loss of some sensitive spec-ies to disturbance is compensated by the invasion of other opportunist species or more generalists. Moreover, in dyn-amic sites under frequent habitat transformation and distur-bance, there is no change in species richness among sites at diﬀerent restoration times, because perturbation events

“re-set” the ant community to the same stage [93].

In this way, as Hoﬀmann [94] has highlighted, the

dis-turbance 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

rela-tionship 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 stud-ies. 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 dis-turbance or restoration is a very desirable tool.

Several of the papers we analyzed described species oc-curring 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

fide-lity 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,

Odonto-machus haematodus, and Pseudomyrmex tenuis (seeTable 2).

Moreover, these ant species might also be generalists, and the choice of better criteria should enable us to distinguish bet-ween 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 Dufrˆene 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

consis-tency is very diﬃcult to assert due to the lack of rigour with

which the ants were related to disturbance or habitats (pre-sence or frequency of occurrence) and the lack of standar-dization regarding the level of disturbance in the papers. The habitats sampled in one paper may be defined as

undistur-bed, which may be diﬀerent from the habitats studied in

ano-ther paper that are defined as more degraded (or less) and should also be defined as an undisturbed habitat. In our

pa-per (includingTable 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,

Cam-ponotus crassus, CamCam-ponotus melanoticus, CamCam-ponotus novo-granadensis, 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,

Pach-ycondyla 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

indica-tors 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,

in-cluding ants, perform under diﬀerent disturbances (see [89,

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[t!]

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]

(14)

Table 2: Continued.

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]

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]

IndVal Forest—vegetation and ground stratum Vasconcelos and

Vilhena [82]

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]

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]

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]

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]

(15)

Table 2: Continued.

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]

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]

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]

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

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]

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]

(16)

Table 2: Continued.

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]

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]

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

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 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]

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]

(17)

Table 2: Continued.

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]

Vilhena [82]

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

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]

Vilhena [82]

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]

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

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

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

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]

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