ECOLOGY, BEHAVIOR AND BIONOMICS

Mini-Winkler Extractor and Pitfall Trap as Complementary Methodsto Sample Formicidae

FHO SILVA1, JHC DELABIE2,3, GB DOS SANTOS4, E MEURER1, MI MARQUES1

1Instituto de Biocincias, Univ Federal de Mato Grosso, Cuiab, MT, Brasil2Lab de Mirmecologia, Centro de Pesquisa do Cacau (CEPEC) CEPLAC, Itabuna, BA, Brasil3Depto de Cincias Agrrias e Ambientais (DCAA), Univ Estadual de Santa Cruz (UESC), Ilhus, BA, Brasil4Fundao Univ Federal do Tocantins, Curso de Cincias Naturais Campus Araguana, Araguana, TO, Brasil

AbstractKeywords

Ant diversity, ground-dwelling ants inventory,landscape, sampling techniques

CorrespondenceFHO Silva, Programa de Ps-graduao emEcologia e Conservao da Biodiversidade,Instituto de Biocincias, Univ Federal deMato Grosso, Av. Fernando Corra da Costa,n.2367, Boa Esperana, 78060-900, Cuiab,MT, Brasil; fabio.silva@svc.ifmt.edu.br

Edited by Wesley AC Godoy ESALQ/USP

Received 29 May 2012 and accepted 13March 2013Published online 26 April 2013

* Sociedade Entomolgica do Brasil 2013

The aim of the present study was to evaluate the use of mini-Winklerextractor and pitfall traps as appropriate and complementary methodsto sample ant communities in the phytophysiognomy mosaic in thePocon Pantanal region, state of Mato Grosso, Brasil. Seven units werestudied for landscape, located within a 25 km2 collection area, formedby thirty 250-m transects, at 1-km intervals in a 55 km area. Fivecollection points were marked in each transect at 50-m intervals, total-ing 150 points. A collection was made at each sampling point with mini-Winkler extractor and pitfall traps. Using the mini-Winkler extractor,1,088 individuals were collected distributed in 20 genera and 55 species,with Solenopsis invicta Buren and Pheidole (gr. biconstricta) sp.1 as themost frequent ants. Using pitfall traps, 2,726 individuals distributed in24 genera and 48 species were sampled and Dorymyrmex (gr. pyrami-cus) sp.1 and Pheidole (gr. biconstricta) sp.1 were the most frequentspecies. A significant difference between the methods was observed inmeasured species number. The Principal coordinates analysis discrimi-nated two species groups exclusively sampled by the mini-Winklerextractor and another by the pitfall methods. Therefore, it was conclud-ed that these methods were complementary for ant diversity invento-ries in the Pocon Pantanal region.

Introduction

Including terrestrial invertebrates in biodiversity and eco-system management inventories has rapidly increasedsince the end of the last century. Inventories of ant specieshave been considered an important tool in studies ontropical biodiversity conservation (Alonso & Agosti 2000).

The abundance and occurrence of ants in almost allterrestrial ecosystems, especially in the tropics, suggestthat their capture is a relatively easy task and that themyrmecofauna can be characterized in a given region usingonly a single and simple sampling method (see, for exam-ple, Souza et al 2012). However, the different research

objectives and the various habitats of ants have markedthe development of a range of methods to capture andstudy them (Bestelmeyer et al 2000, Delabie et al 2000a,Sarmiento 2003).

Methods commonly used for litter ant inventories in-clude fall traps, extraction from the litter, and sampling bysquares and bait (Olson 1991, Bestelmeyer et al 2000).Fisher (1999) and Alonso & Agosti (2000) considered themini-Winkler extractor a technique that could be easilystandardized for myrmecofauna inventories. However, thismethod favors small-sized, cryptic species or species withlittle mobility that live in habitats where litter has accumu-lated (Bestelmeyer et al 2000), such as tropical forests.

Neotrop Entomol (2013) 42:351358DOI 10.1007/s13744-013-0131-7

In contrast, fall traps, such as the pitfall trap, can beused because it is also a method considered suitable forcapturing invertebrates that are more active in the soil,including Formicidae (Spence & Niemel 1994, Bestelmeyeret al 2000). Furthermore, this collecting technique is con-sidered as complementary to sampling by the mini-Winklerextractor method (Delabie et al 2000a). Another factor tobe considered is that this method seems more indicatedfor arid regions and open areas with little plant cover andthin litter (Fisher 1998), the situation found in the studyarea of the present research, because the efficiency of antcollection methods depends essentially on the habitat un-der study (Romero & Jaff 1989).

The Pantanal is considered one of the largest wetlands inLatin America, formed by a mosaic of different communitieswith abrupt changes in its landscape (Prance & Schaller 1982),resulting in interactions between edaphic, hydrologic, andbiogeographical factors (Lourival et al 2000).

Thus, the objective of the present study was to analyze thecomplementariness between the mini-Winkler extractor andpitfall trap collectionmethods, as suitable techniques to assessthe composition of the Formicidae community in the PoconPantanal region, considering the phytophysiognomic varia-tions of this region and the specificities of the methods used.

Material and Methods

Study area

The study was carried out in the Cuiab-Bento Gomes-Paraguaizinho Pantanal, called the Pocon Pantanal, inthe location of Pirizal (161524S to 175432S, 563624W to 575623W), municipality of Nossa Senhora do Livra-mento, state of Mato Grosso, Brasil. Sampling was carriedout during November 2005 during the dry season withlittle rainfall in the region.

The Pocon Pantanal region is formed by several phyto-physiognomies that provide a set of varied habitats that wereclassified in the present study according to Veloso et al (1991),PCBAP (2007), Silva et al (2000), Santos et al (2004) andNunes-da-Cunha et al (2007). Five environments were sam-pled; the Landi and Cambarazal were characterized as forestareas while natural fields, natural open fields, and pastureswere characterized as open areas.

Landi. This formation is characterized by a low and continu-ous canopy with individual height varying from 3 to 7.5 m andis associated with the water courses. The sinsia tree veg-etation is dominated by Licania parviflora (Chrysobalanaceae),Calypthrantes eugenioides (Myrtaceae), Mabea sp.(Euphorbiaceae), and Calophyllum brasiliense (Crusiaceae)(Nunes-da-Cunha et al 2010).

Cambarazal. This formation corresponds to a dense homo-geneous flooding area, where cambar (Vochysia divergens(Vochysiaceae), predominates an Amazon species thatvaries from 5 to 18 m in height, and that is a colonizer offlooded natural fields in the Pantanal of PoconMT. Itslocal distribution is probably due to the seeds coming fromindividual specimens located in nearby riparian forests(Nunes-da-Cunha et al 2010).

Natural fields. These represent about 30% of the vegetationin the Pantanal (Silva et al 2000) where the murundu fieldsare inserted, made up of flat areas which are flooded in therainy season and where there are countless little hills(murundu), susceptible to flooding when there is extremeflood. The flat areas and the smaller murundus are coveredby rustic vegetation and the largest areas by woody Cerradovegetation. Termite activities and erosion processes seem toshape themurundus into a rounded or elliptical form, with 12 m maximum in height (Nunes-da-Cunha et al 2010).

Natural open fields. They are characterized by the mimosopasture grass Axonopus purpusii (Poaceae), a perennial vege-tation resistant to temporary submersion. Widely distributedthroughout the Pantanal, they occur in cerrado fields on theedges of bays (permanent and temporary), and mainly inareas of seasonal open fields in the sandy Pantanal areas(Nunes-da-Cunha et al 2010).

Pastures. These regions are basically made up of Brachiariahumidicola (Poaceae) grass originally from Africa which adaptedwell to Brasil, mainly in waterlogged soils. In these areas, thereare also pasture fields which are not periodically renewed,where there is a mixture of B. humidicola and A. purpusii, andare known as mixed fields (Nunes-da-Cunha et al 2010).

Field procedures

The ant community was sampled using mini-Winkler extractor(Fisher 1998, Bestelmeyer et al 2000) and pitfall traps (Adis2002). Twenty-nine 250-m transects were marked at intervalsof 1 km in an area of 25 km2, following the Rapid AssessmentProtocols and Long-Term Ecological Research, which allowsnontendentious estimates of the distribution, abundance, bio-mass, and biogeography of the species among sites studied(Fig 1) (Magnusson et al 2005). Of the transects sampled,three were marked in the Landi, two in the Cambarazal, fourin theMurundu field, 13 in the natural open field and seven inthe pasture phytophysiognomies. Each transect characterizeda sample point where five collections of 1 m2 litter were madewith themini-Winkler extractor and then five pitfall traps wereinstalled. An interval of 50 m was established between eachcollection point to guarantee sampling independence because

352 Silva et al

the probability of collecting ants of the same colony in twosuccessive samples is then remote and, according to Baccaroet al (2011), subsamples with a minimum distance of morethan 10 m can collect a more diverse number of species.

Each pitfall trap was installed for 48 h at each samplingpoint and the litter samples were suspended for 72 h in themini-Winkler extractor in a covered environment at envi-ronmental temperature (Bestelmeyer et al 2000).

Laboratory procedures

Ants were screened and identified at taxonomic level ofthe genus, species, and/or morphospecies level followingBolton et al (2006), Baroni-Urbani & Andrade (2007), andLaPolla et al (2010). Vouchers were deposited at the Cole-o de Referncia Entomolgica, Laboratrio de Taxonomiae Ecologia de Artrpodes, Universidade Federal de MatoGrosso.

Data analyses

Only workers and their absolute frequency were assessedin the data analysis. According to Romero & Jaff (1989),the capture measurement units of fauna surveys should beat least equivalent. Thus the capture frequency, the

measurement used in this study, substituted abundancein comparisons between the methods to estimate theprobability of finding a determined species in the studylocation and reduced the effect of abundance of the socialinsects in the species spatial distribution studies. Accordingto Hughes (1986) and Longino (2000), for social groups, thenumber of individuals per se is a weak and erroneousmeasurement, because using the mini-Winkler extractorand pitfall traps in an area where ants with massive re-cruitment behavior occur, such as the army ants, Pheidoleor Solenopsis species, would give tendentious results thatdo not represent the local community.

The species number was compared to the estimatedspecies number using three species richness estimators,Jackknife 1, the ChaoJaccard similarity index, and the indexbased on the concept of cover of the sample, and speciesaccumulation and rarefaction curves were constructed usingthe EstimateS version 7.5 software (Cowell 2005).

The nonparametric statistical KruskalWallis methodwas used to compare the number of species per sampleamong the methods in each environment and among theenvironments in each method using the STATISTICA version7 software.

Ants were classified by functional guild according toSilvestre et al (2003) and Brando et al (2009). The

Fig 1 The 25 km2 plot used tocollect ants in thephytophytophysiognomymosaic of the Pocon Pantanal,MT, Brasil. Source:Geoprocessing Laboratory ofthe Pantanal Study Nucleus(NEPA) UFMT adapted fromGoogle Earth. Letters (A, B, C,D, E, F) and numbers (1, 2, 3, 4,5) represent trails northsouthand eastwest, respectively.Letters and numbers (A1, A2,A3) indicate the transectlocation.

Complementary Methods to Sample Formicidae 353

EstimateS software (Cowell 2005) version 7.5 was used tocalculate the ChaoJaccard similarity coefficient (Chao et al2005) among collection methods.

The principal coordinate analysis (PCoA) was used toassess whether there was a pattern in the species distribu-tion between the two methods, using capture frequencydata standardized by traps and calculations based on theBray Curtis similarity measurement using the Principal Co-ordinate Analysis software (Anderson 2003).

Results

A total of 3,814 Formicidae individuals were obtained bythe pitfall trap and mini-Winkler extractor methods, dis-tributed in 33 genera and 73 species, with Pheidole(Westwood), Solenopsis (Westwood), Camponotus (Mayr),and Hypoponera (Santschi) presented the greatest richness(see Electronic Supplementary Material; ESM). Pitfall traps(2,726 individuals) allowed the collection of nearly threetimes more ants than the mini-Winkler extractor (1,088individuals). Twenty genera and 55 species were sampledwith the mini-Winkler extractor as compared to the 24genera and 48 species collected with the pitfall traps.Pheidole and Solenopsis commonly represented in bothmethods, while Camponotus appeared as one of the rich-est genus in the pitfall traps and Hypoponera in the mini-Wrinkler method (see ESM).

Solenopsis invicta (Buren) (16 occurrences), Pheidole(gr. biconstricta) sp.1 (14 occurrences), Brachymyrmex cf.heeri (12 occurrences), Nylanderia sp.1 (11 occurrences),and Solenopsis (gr. globularia) sp.1 (10 occurrences) werethe most frequent using the mini-Winkler (see ESM).

Dorymyrmex (gr. pyramicus) sp.1 (26 occurrences), Phei-dole (gr. biconstricta) sp.1 (22 occurrences), S. invicta (19occurrences), and Pheidole sp.10 (16 occurrences) were themost frequent using the pitfall traps (see ESM).

Using the mini-Winkler extractor, 442 individuals weresampled in the forest environment, which were distributedin 15 genera and 26 species. Solenopsis (4 spp.), Nylanderia(3), and Hypoponera (3) presented the greatest richness.Using pitfall traps, 209 individuals, 11 genera, and 21 specieswere sampled; Pheidole (4), and Solenopsis (3) were thegroups with the greatest number of species (see ESM).

Using the mini-Winkler, 646 individuals were sampled innatural open fields, which were distributed in 22 generaland 47 species. Pheidole (6 spp.) and Solenopsis (5) werethe genera with greatest richness. Using pitfall traps, 2,545individuals were sampled, 26 general and 46 species. Phei-dole (7 spp.), Solenopsis (5), and Camponotus (4) were thegroups with the greatest number of species (see ESM).

No significant differences were observed between themethods regarding the number of species when assessed

Fig 2 Box plot of the KruskalWallis non parametrical analysis. Com-parison of the species number between the pitfall trap andmini-Winklermethods in forest environment (a) and open fields (b). Comparison ofthe species number between environments using pitfall (c) and mini-Winkler (d). The horizontal line indicates the average value, the boxcorresponds to the percentile (2575%) values, whisker represents theminimum and maximum values of the whole sampling.

354 Silva et al

in the forest environment (KruskalWallis=0.1012; df=1, 10;P=0.7503) (Fig 2a). However, there was significant differ-ence when the number of species was assessed in thenatural open fields (KruskalWallis=14.0879; df=1, 48;P=0.0002) (Fig 2b). When the performance of eachmethod was analyzed in relation to the environment,no significant difference was observed when the num-ber of species collected by pitfall traps was comparedamong the environments (KruskalWallis=9.1879; df=1, 29;P=0.6582) (Fig 2c). A similar pattern was observed when theresults obtained for the mini-Winkler were assessed (KruskalWallis=3.5656; df=1, 29; P=0.0590) (Fig 2d).

An application of the richness estimators showed that55 species were sampled by the mini-Winkler extractorand 48 using the pitfall traps (Table 1). The associationamong the methods showed that 73 species were ob-served, indicating a good complementariness of thesemethods for the number of species collected (Table 1).This complementariness can also be observed when thespecies accumulation curve is analyzed. A larger numberof species is collected with a smaller number of sampleswhen methods are associated compared to the resultsobtained using isolated methods (Fig 3). Furthermore, a0.67 coefficient similarity was observed between methodsusing the ChaoJaccard Index.

A 22.5% variation was observed in the data using thePCoA, which can be explained by the differences betweenthe methods used in sampling this community. Two groupsof species were defined, one that predominated in thesampling with the mini-Winkler extractor and the otherwith the pitfall trap (Fig 4).

Discussion

The efficiency of the complementariness between the twocollection methods applied in the present study for theobserved and estimated richness among the ant commu-nity was previously tested in an ant diversity study on theisland of Madagascar (Fisher et al 2000) and were essentialto reinforce the importance of complementariness amongthese methods. Studies that proved that a number ofspecies were collected by the mini-Winkler extractor thanby the pitfall trap in the Brazilian Atlantic Rainforest whenefficient sampling of ant communities is desired (Delabie etal 2000b, Orsolon-Souza et al 2011).

Our data for the Pocon Pantanal region corroboratedfindings by Delabie et al (2000b) because the mini-Winkleris a method that samples a greater number of Formicidaespecies, especially small sized and the cryptobiotic ones,

Table 1 Observed and estimated ant species richness in different phytophysiognomies collected by different methods in the Pocon Pantanal,MT, Brasil. Number of species observed, number of species after rarefaction (Coleman method), number of species estimated by Jackknife I, andChao 2, index based on the sample cover index (ICE). Values in parentheses correspond to the standard error.

Sample methods Observed and estimated ant species richness

Observed Rarefaction Jackknife 1 Chao 2 ICE

Pitfall trap 48 47.7 (0.6) 61.5 (4.5) 60.5 (7.9) 60.7 (0.01)

Mini-Winkler 55 54.2 (0.9) 82.0 (9.2) 95.6 (17) 99.3 (0.1)

Pitfall Trap+mini-Winkler 73 72.3 (0.8) 101.0 (10.5) 103.2 (12.8) 114.1 (0.01)

Fig 3 Accumulation curve ofthe number of Formicidaespecies collected in differentphytophysiognomies in thePocon Pantanal, MT, Brasil,using the mini-Winklerextractor and pitfall traps.Captions: dashed line observedrichness, filled circle mini-Winkler, filled square pitfalltrap, filled diamond mini-Winkler, plus sign pitfall trap.

Complementary Methods to Sample Formicidae 355

such as Hypoponera spp., Strumigenys denticulata (Mayr),Strumigenys subdentata (Mayr), and Oxyepoecus vezenyii(Forel). This data demonstrates the need of its use whencollecting in the soils in the Mato Grosso Pantanal. How-ever, ants with large and wide dispersion throughout theenvironment can be subsampled by this method. Thislimitation can, however, be compensated by the use ofthe pitfall trap because this method depends on the dailyforaging activity of the ants (Adis 2002).

According to Bestelmeyer et al (2000), the pitfall trapalso has limitations when sampling slow-moving speciesand those with cryptobiotic behavior. Thus, it was ob-served that the limitations of one method can be mitigatedby the attributes of another.

The results obtained by the ChaoJaccard similarity in-dex showed that the two methods used collected partiallysimilar groups of ants. The similarity observed was justifiedby the generalist characteristics, dominance, and widedistribution of some species found in the area sampled.For example, Brachymyrmex cf. heeri had 12 records withthe mini-Winkler extractor and 13 with the pitfall traps (seeESM). This occurrence was justified by the undergroundopportunistic habit of the ant that constructs its nests invarious locations and forages over extensive areas (Fernndez2003, Silvestre et al 2003).

In addition to this species, S. invicta, Solenopsis(gr. globularia) sp.1, Nylanderia sp.1, Pheidole (gr. bicon-stricta) sp.1, and Camponotus abstinens (Forel), consideredgeneralists and dominant in the soil and vegetation), werealso sampled by the two methods (Fernndez 2003,Silvestre et al 2003).

However, the PCoA and the similarity index reflectedthe difference in species composition between the meth-ods used. For example, Hypoponera (5 spp.) was sampledonly with the mini-Winkler extractor while Dorymyrmex (2),

and Pogonomyrmex naegelii (Emery) were captured veryfrequently by the pitfall traps (see ESM). Hypoponera arecommon inhabitants of decaying wood, trunks, and hollowbranches fallen on the ground and especially of the litter(Lattke 2003) which favors its capture by the mini-Winklerextractor.

In addition, Cyphomyrmex sp.3, Cyphomyrmex sp.4,Gnamptogenys striatula (Mayr), S. denticulata Mayr, S.subdentata Mayr, Rogeria blanda (Smith), Trachymyrmexfuscus (Emery), and Trachymyrmex iheringi (Emery) weresampled exclusively with the mini-Winkler extractor (seeESM). These taxa are frequently cryptic, litter inhabitants(Fernndez 2003, Silvestre et al 2003), and this methodwas especially efficient in sampling habitats with greaterlitter accumulation.

The cryptobiotic O. vezenyii (Forel) was exclusively sam-pled by the mini-Winkler extractor (see ESM), and thefrequency crytobiotic species have been collected in faunasurveys has increased because of the development of litterextraction techniques (Albuquerque & Brando 2004,Castilho et al 2007).

Species collected mainly by pitfall traps, such as Dory-myrmex sp.1, Dorymyrmex (gr. Pyramicus) sp.1, and P.naegelii, build their nests in the soil in arid and semiaridregions, preferring open habitats with little plant cover(Cuezzo 2003, Fernndez 2003). Thus the higher capturefrequencies of these taxa with pitfall traps corroborateddata by Fisher (1999), who considered this method ideal forarid regions and open areas with little plant coverage.

In addition to these ants, Acromyrmex fracticornis(Forel), Acromyrmex subterraneus (Forel), and Atta laevi-gata (Smith) were sampled only by pitfall traps. Thesespecies are common inhabitants of open Cerrado (centralBrasil savanna) areas with little litter (Silvestre et al 2003),similar to the field areas we sampled.

Fig 4 Indirect ordination axisof the ant community samplein the phytophysiognomicalmosaic of the Pocon Pantanal,Mato Grosso, Brasil, using themini-Winkler extractor andpitfall trap methods. Captions:filled diamond mini-Winkler,plus sign pitfall trap.

356 Silva et al

The association of techniques used in the present studywas more efficacious in sampling in regions such as thePocon Pantanal because the mini-Winkler extractor fa-vored species collection in habitats with accumulated litterwhile the pitfall trap favored sampling in locations withlittle plant cover and thin litter. Therefore, pitfall trapsshould be used in association with mini-Winkler extractorsalso because pitfall traps are efficient in sampling in openfield areas, unlike the extractor that requires the accumu-lation of litter for a good performance in the sampling ofsoil ants. Thus, combined the use of these sampling meth-ods contemplates the characteristic of the environment onthe spatial scale assessed and the bioecological peculiari-ties of ants in the region studied.

Other studies, such as in Costa Rica, have reported thatpitfall traps captured generalist species with a larger bodysize, which occurs less frequently when methods with litterextraction are used (Olson 1991). This pattern was alsoobserved in the present study, for example, for the Poner-inae Odontomachus bauri (Emery), Odontomachus brun-neus (Patton), and Pachycondyla harpax (Fabricius).Because of their body sizes (1 cm or more) and the diam-eter of the pitfall trap, these ants were exclusively collect-ed by this technique.

However, if the study is to focus only on open areassuch as natural fields and introduced grass pastures, thepitfall trap associated to bait and hand collection is anefficient method for a satisfactory sampling, as long astraps remains in the field for a period longer than 48 h.However, if sampling is carried out for a short period oftime, the mini-Winkler extractor is the suggested methodto be associated with pitfall traps for the efficient collectionof the highest number of species and functional groups.

Assessment of the complementariness of the two meth-ods in forested and open areas using the concept of func-tional groups showed that the results between themethods differed in the composition of the genera collect-ed. For example, predator and generalist ants were morefrequently collected by pitfall traps in open areas. Thus, themini-Winkler extractor favors smaller and less active spe-cies among the functional groups while the pitfall trapfavors those that are larger and mobile (see ESM).

It was observed, therefore, that the results of the pres-ent research are important for knowledge on the soil andlittle ant community in the Pantanal biome, since this wasthe first study to use the association of the pitfall trap andmini-Winkler extractor collection methods for this region.

Acknowledgments This paper is dedicated to the memory of the lateProfessor Dr. Joachim Adis for his dedication to the study of arthropods inthe Pantanal of Mato Grosso who passed his knowledge on to theteaching staff, employees, and students of the Laboratrio de Taxonomiae Ecologia de Artrpodes, Universidade Federal do Mato Grosso. Theauthors also thank Professor Dr. Carlos Roberto Ferreira Brando,

Dr. Rodrigo Feitosa, and Dr. Rogrio Rosa da Silva for their help in theidentification of the specimens sampled here. The authors also thank thestudents and the technician of the Francisco de Assis Rondon of theLaboratrio de Taxonomia e Ecologia de Artrpodes, Universidade Federaldo Mato Grosso for their help in the field collections. We finally thank thePrograma de Ps-graduao em Ecologia e Conservao da Biodiversidadedo Instituto de Biocincias da UFMT, Centro de Pesquisas do Pantanal(CPP), Ncleo de Pesquisas do Pantanal (NEPA), and the Programa dePesquisas em Biodiversidade (PPBio) for logistic help. Thanks are due tothe CNPq for the fellowships and research grants to the first two authors.

Electronic supplementary material The online version of this article(doi:10.1007/s13744-013-0131-7) contains supplementary material, whichis available to authorized users.

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Mini-Winkler Extractor and Pitfall Trap as Complementary Methods to Sample FormicidaeAbstractIntroductionMaterial and MethodsStudy areaField proceduresLaboratory proceduresData analyses

ResultsDiscussionReferences