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Comparison between Winkler's extractor and pitfall traps to estimate leaf litter ants richness (Formicidae) at a rainforest site in southest Brazil.

Comparacao entre extrator de Winkler e armadilha de queda para estimar a riqueza em especies de formigas (Formicidae) de serapilheira em floresta tropical do sudeste do Brasil

1. Introduction

Species richness is a central topic in community ecology (Longino et al., 2002) and a fundamental component of biodiversity (Gaston, 1996). However, it is difficult to estimate the species richness of a given area, since the available techniques do not always provide a representative sample of the total richness (Agosti et al., 2000; Agosti and Alonso, 2001).

Studies on communities of leaf litter arthropods (e.g. Romero and Jaffe, 1989; Parr and Chown, 2001) point out the need for well-structured sampling protocols to properly estimate richness and evenness. In the case of ants, foraging area, nest dispersion, and activity patterns are important factors that must be considered in a sampling design (Wang et al., 2001). Researchers of ant communities suggest the combination of different techniques as the best way to estimate richness and abundance of ants (Delabie et al., 2000; Longino et al., 2002).

Pitfall traps, Winkler's extractors, food baits and hand collecting are the most efficient techniques, and, hence, the most frequently used in ant community studies. Both Winkler's extractors and pitfalls have proven to be efficient in sampling abundance and richness of leaf litter ant communities (Romero and Jaffe, 1989; Wang et al., 2001). However, Parr and Chown (2001) compared both techniques and suggested that species sampled with Winkler's extractors are more abundant and smaller than those sampled with pitfalls.

It is also possible to use data obtained with both techniques to estimate species richness. Species accumulation curves allow estimating sample completeness (Colwell and Coddigton, 1994), assessing the efficiency of the method used, and comparing different inventories (Soberon and Llorente, 1993).

Therefore, it is important to compare in the same site the efficiency of the two most used techniques for sampling ant diversity. We studied communities of leaf litter ants from the Brazilian Atlantic Forest, compared richness estimates for genera and species, and built species accumulation curves with data from pitfall traps and Winkler's extractors.


2. Materials and Methods

2.1. Study area

This study was carried out in Dense Ombrophylous Forest (IBAMA, 1996), in the "Reserva Biologica do Tingua" (ReBio Tingua, 22[degrees]28'-22[degrees]39' S and 43[degrees]13'-43[degrees] 34' W), Nova Iguacu municipality, state of Rio de Janeiro, in November 2003. Sampling was carried out in submontane rainforest (Veloso et al., 1991) at 400 m asl on average.

2.1.1. Characterisation of submontane rainforest

Submontane rainforest presents canopy height varying from 15 to 20 m on average, discontinuous in some places and where Rubiaceae, Mimosoideae, Myrtaceae and Lauraceae are the most speciose families (Rodrigues, 1996). Understory is relatively dense with high frequency of small trees and bushes. Herbaceous climbers and lianas are common, particularly at the forest edge. Some epiphytes like Orchidaceae, Bromeliaceae, Araceae and Cactaceae species are relatively frequent close to streams (IPJBRJ, 2002) (Figure 1).

2.2. Sampling

Winkler's Extractors (Wke): We marked 25 points along a 1,200 m transect, and at each point we stretched two perpendicular 25 m lines; one to the left and the other to the right. At the end of each line we delimited a 1 [m.sup.2] plot, totalling 50 plots. Sifted samples from each plot were separated and placed into Winkler's extractors for 48 hours. This procedure was adapted from Delabie et al. (2000).

Pitfall traps (Pft): We use 50 pitfalls that were distributed along the previously described transect, between the plots with Winkler's extractors. Pitfalls consisted of 300 mL plastic glasses with a diameter of 7.0 cm, containing 3% formalin. Pitfalls were buried in the soil with the upper border parallel to the ground, and remained open for 48 hours.

2.3. Identification of ants

Ant genera were identified following Bolton (1994), and subfamilies following Bolton (2003). Whenever possible, identification at species level was carried out with keys from taxonomical reviews or by comparison with identified specimens from the Entomological Collection Angelo Moreira da Costa Lima (CECL), at the Institute of Biology of the Universidade Federal Rural do Rio de Janeiro, Brazil. Vouchers were deposited in the same collection.

2.4. Data analysis

Species accumulation curves were built using the number of samples (Soberon and Llorente, 1993). According to Moreno and Halffter (2000) and Medellin (1993), this method is better for sampling units that grow linearly.

For each technique, the total of species per sample was randomised 1,000 times in the program EcoSim[R] (Gotelli and Entsminger, 2009) to estimate confidence intervals (adapted from Lourenco et al., 2010). Accumulation curves were built from observed and randomised data. Logarithmic functions for the randomised curves of each technique were also presented.

3. Results and Discussion

In total, we collected ants from ten subfamilies, 37 genera and 105 species (Table 1). Those two methods resulted in a satisfactory sampling of richness; 21.3% of the genera and 47.6% of the species were collected exclusively with Winkler's extractors, whereas 6.4% of the genera and 9.5% of the species were collected exclusively with pitfalls (Table 2).


Myrmicinae was the most frequent ant subfamily sampled with both techniques, and this result is probably related to the high richness and abundance of this group in the leaf litter fauna of the Neotropics (Silva and

Brandao, 1999). Veiga-Ferreira et al. (2005) and Vargas et al. (2007) recorded a high number of species of Myrmicinae in the Atlantic Forest and the Restinga of Rio de Janeiro, respectively. For each of the subfamilies Cerapachyinae and Ecitoninae, only one species was sampled with Winkler's extractors and pitfalls. This result is probably related to habitat conditions that can affect the structure of the ant community (Andersen, 2000; Holldobler and Wilson, 1990; Nakamura et al., 2003), and consequently the frequency of each species. According to Lassau and Hochuli (2004), the structural complexity of the environment directly affects species richness.

Although pitfall traps tend to capture larger ants (Olson, 1991), such as the specimens of Ectatomminae and Ponerinae recorded in the present study, they can also sample abundance and richness of the leaf litter ant community (Romero and Jaffe, 1989; Wang et al., 2001). Winkler's extractors captured smaller and cryptic leaf litter ants, such as the Myrmicinae, or even ants that are rarely collected with other techniques (Bestelmeyer et at., 2000; Castilho et al., 2007). For the Atlantic Forest, Winkler's extractor had proven to be the most efficient single sampling technique to estimate richness. However, pitfalls also recorded a significant portion of the total richness. Lassau and Hochuli (2004) collected ants using only pitfalls in complex environments, and, although those environments were different from the one studied here, ant richness was higher in environments with more complex structures. Therefore, pitfalls must be used together with other sampling techniques in the field, especially in tropical forests.

On the one hand, our results are consistent with Parr and Chown (2001), who, when comparing sampling techniques, suggested that species collected with Winkler's extractors are more abundant and smaller than the ones collected in pitfalls. On the other hand, Olson (1991) showed that Winkler's extractors and pitfalls together can sample c. 75.0% of the species richness estimated for the leaf litter ant fauna, a percentage considered reasonable for ecological studies on leaf litter.

Despite differences in efficiency, species accumulation curves for both techniques were similar (y = 19.743 Ln(x) + 19.962; [r.sup.2] = 0.9688; p < 0.001 for Wke, y = 14.487 Ln(x) - 3.348; [r.sup.2] = 0.995; p < 0.001 for Pft), as well as the curve obtained with both methods combined (y = 22.378 Ln(x) + 20.575; [r.sup.2] = 0.9739; p < 0.001 for Wke + Pft) (Figure 2). To obtain the total of 105 species recorded with both techniques combined, it would be necessary to take 64.07 samples with Wke and 111.84 with Pft. Therefore, we noticed that Winkler's extractors were c. 74.0% more efficient than pitfalls in the Atlantic Forest, corroborating results from Parr and Chown (2001).

Sampling techniques must be used with a well-structured sampling design in order to advance knowledge on the ant fauna of Brazilian biomes, especially in the leaf litter (Castilho et al. (2007) and Veiga-Ferreira et al. (2010) for new records of ant's species), allowing more complete environmental analyses. The influence of ants on edaphic processes, flux of energy and matter in ecosystems (Brown, 1997), predation, and seed dispersal (Folgarait, 1998; Passos and Oliveira, 2002, 2003; Leal, 2003) makes this insect group a good study model for environmental surveys and monitoring (Silva and Brandao, 1999).

Acknowledgements--We are grateful to the team at the Reserva Biologica do Tingua (Nova Iguacu office) and to IBAMA for the study license. This study was supported by grants from the Brazilian governmental to GOS (CAPES), to AJMN and CELS (CNPq).


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Orsolon-Souza, G. (a) *, Esberard, CEL. (b), Mayhe-Nunes, AJ. (b), Vargas, AB. (c), Veiga-Ferreira, S. (a), and Folly-Ramos, E. (d)

(a) Programa de Pos-graduacao em Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro--UFRRJ, Rod. BR 465, Km 7, CEP 23890-000, Seropedica, RJ, Brazil

(b) Departamento de Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro--UFRRJ

(c) Programa de Pos-graduacao em Ciencias Ambientais e Florestais, Instituto de Florestas, Universidade Federal Rural do Rio de Janeiro--UFRRJ

(d) Departamento de Engenharia e Meio Ambiente, Universidade Federal da Paraiba--UFPB, R. Manoel Goncalves, s/n, CEP 58297-000, Rio Tinto, PB, Brazil

* e-mail:

Received July 19, 2010--Accepted November 11, 2010--Distributed November 30, 2011 (With 2 figures)
Table 1. List of species collected by Winkler's extractor and pitfall
traps in submontane rainforest in "Reserva Biologica do Tingua", Rio
de Janeiro state, Brazil. November/2003.

Subfamilies        Species/Morphospecies        Winkler's   Pitfall
                                                extractor    traps

Amblyoponinae      Amblyopone armigera Mayr,        #          #
                   Amblyopone elongata              #          #
                     (Santschi, 1912)
                   Prionopelta punctulata           #          -
                     Mayr, 1866

Ceraphachynae      Cerapachys splendens             #          -
                     Borgmeier, 1957

Dolichoderinae     Azteca sp.1                      -          #
                   Linepithema pulex Wild,          #          -
                   Linepithema sp.1                 #          #

Ecitoninae         Labidus sp.1                     -          #

Ectatominae        Ectatomma permagnum              #          -
                     Forel, 1908
                   Ectatomma edentatum              #          -
                     Roger, 1863
                   Ectatomma brunneum F.            -          #
                     Smith, 1858
                   Gnamptogenys cf. horni           #          -
                   Gnamptogenys horni               #          #
                     Santschi, 1929
                   Gnamptogenys rastrata            #          #
                     (Mayr, 1866)
                   Gnamptogenys cf.                 #          -
                   Gnamptogenys cf.                 #          -
                   Gnamptogenys sp.1                -          #

Formicinae         Brachymyrmex sp.1                #          -
                   Brachymyrmex sp.2                #          #
                   Brachymyrmex sp.3                #          #
                   Camponotus                       #          -
                     novogranadensis Mayr,
                   Camponotus punctulatus           #          -
                     Mayr, 1868
                   Campontous sp.1                  #          -
                   Camponotus sp.2                  -          #

Myrmicinae         Acromyrmex aspersus (F.          #          -
                     Smith, 1858)

Attini             Acromyrmex coronatus             #          -
                     (Fabricius, 1804)
                   Acromyrmex niger (F.             #          -
                     Smith, 1858)
                   Apterostigma sp.1                #          #
                   Apterostigma sp.2                #          #
                   Cyphomyrmex gr. strigatus        #          #
                   Cyphomyrmex gr. strigatus        #          #
                   Cyphomyrmex gr. rimnosus         #          -
                   Mycocepurus smithii Forel,       #          #
                   Mycetarotes carinatus            #          -
                     Mayhe-Nunes, 1995
                   Sericomyrmex sp.1                #          #
                   Sericomyrmex sp.2                #          #
                   Sericomyrmex sp.3                #          #
                   Trachymyrmex sp.1                #          #

Myrmicinae         Basiceros bruchi Santschi,       #          -

Non-Attini         Basiceros disciger (Mayr,        #          -
                   Basiceros iheringi               #          -
                     (Emery, 1887)
                   Basiceros rugiferum              #          #
                     (Mayr, 1887)
                   Carebara urichi (Wheeler,        #          #
                   Crematogaster nigropilosa        #          -
                     Mayr, 1870
                   Hylomyrma balzani (Emery,        #          -
                   Hylomyrma reitteri (Mayr,        #          #
                   Lachnomyrmex plaumanni           #          -
                     Borgmeier, 1957
                   Megalomyrmex drifti Kempf,       #          #
                   Megalomyrmex goeldii             #          #
                     Forel, 1912
                   Megalomyrmex silvestrii          #          -
                     Wheeler, 1909
                   Oxypoecus sp.1                   #          #
                   Oxypoecus sp.2                   #          -
                   Pheidole sp.1                    #          #
                   Pheidole sp.2                    #          #
                   Pheidole sp.3                    #          #
                   Pheidole sp.4                    #          #
                   Pheidole sp.5                    #          #
                   Pheidole sp.6                    #          #
                   Pheidole sp.7                    #          #
                   Pheidole sp.8                    #          #
                   Pheidole sp.9                    #          -
                   Pheidole sp.10                   #          -
                   Pyramica sp.1                    #          #
                   Pyramica sp.2                    #          #
                   Pyramica sp.3                    #          -
                   Pyramica sp.4                    -          #
                   Rogeria sp.1                     #          -
                   Rogeria sp.2                     #          -
                   Rogeria sp.3                     #          -
                   Solenopsis sp.1                  #          #
                   Solenopsis sp.2                  #          #
                   Solenopsis sp.3                  #          -
                   Solenopsis sp.4                  #          #
                   Solenopsis sp.5                  #          -
                   Solenopsis sp.6                  #          #
                   Solenopsis sp.7                  #          -
                   Strumigenys elongata             #          -
                     Roger, 1863
                   Wasmannia auropunctata           #          #
                     (Roger, 1863)
                   Wasmannia lutzi Forel            #          #

Ponerinae          Anochetus mayri Emery,           #          -
                   Centromyrmex sp.1                -          #
                   Hypoponera sp.1                  #          #
                   Hypoponera sp.2                  #          -
                   Hypoponera sp.3                  #          -
                   Hypoponera sp.4                  #          -
                   Hypoponera sp.5                  #          -
                   Hypoponera sp.6                  #          -
                   Leptogenys sp.1                  #          -
                   Odontomachus chelifer            #          #
                     (Latreille, 1802)
                   Odontomachus haematodus          -          #
                     (Linnaeus, 1758)
                   Odontomachus meinerti            #          -
                     Forel, 1905
                   Odontomachus sp.1                #          -
                   Pachycondyla bucki               #          -
                     (Borgmeier, 1928)
                   Pachycondyla ferruginea          #          -
                     (F. Smith, 1858)
                   Pachycondyla harpax              #          #
                     (Fabricius, 1804)
                   Pachycondyla stigma              #          #
                     (Fabricius, 1804)
                   Pachycondyla striata F.          #          #
                     Smith, 1858
                   Pachycondyla venusta             #          #
                     Forel, 1912
                   Thaumatomyrmex mutilatus         #          -
                     Mayr, 1887

Proceratiinae      Discothyrea sexarticulata        #          #
                     Borgmeier 1954
                   Proceratium brasiliense          #          -
                     Borgmeier, 1959

Pseudomyrmecinae   Pseudomyrmex sp.1                #          -
                   Pseudomyrmex sp.2                #          -
                   Pseudomyrmex sp.3                -          #
                   Pseudomyrmex sp.4                -          #

# = collected by the technique; - = non-collected by the technique.

Table 2. Distribution of genera and species richness of each
Formicidae subfamilies sampled by Winkler's extractor (Wke) and
pitfall traps (Pft) at "Rebio Tingua", Brazil, November/2003.

Subfamily                        Genera                  Species

                      Wke         Pft         Common       Wke

Amblyoponinae       2    (1)     1    (-)       1        3    (1)
Cerapachyinae       1    (1)    --    --        --       1    (1)
Dolichoderinae      1    (-)     2    (1)       1        2    (1)
Ecitoninae          --    --     1    (1)       --       --    --
Ectatomminae        2    (-)     2    (-)       2        7    (5)
Formicinae          2    (-)     2    (-)       2        6    (4)
Myrmicinae          20   (4)     9    (-)       14       54   (23)
Ponerinae           6    (3)     4    (1)       3        20   (12)
Proceratiinae       2    (1)     1    (-)       --       2    (1)
Pseudomyrmecinae    1    (-)     1    (-)       1        2    (2)
Total               37   (10)   23    (3)       24       97   (50)

Subfamily                Species

                     Pft         Common

Amblyoponinae      2    (-)        2
Cerapachyinae      --    --        --
Dolichoderinae     2    (1)        1
Ecitoninae         1    (1)        --
Ectatomminae       4    (2)        2
Formicinae         3    (1)        2
Myrmicinae         32   (1)        31
Ponerinae          8    (2)        6
Proceratiinae      1    (-)        1
Pseudomyrmecinae   2    (2)        --
Total              55   (10)       45

Exclusive genera and species for each technique are within
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Author:Orsolon-Souza, G.; Esberard, C.E.L.; Mayhe-Nunes, A.J.; Vargas, A.B.; Veiga-Ferreira, S.; Folly-Ramo
Publication:Brazilian Journal of Biology
Date:Nov 1, 2011
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