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CONSERVATION BIOLOGY AND BIODIVERSITY Ground Ant Diversity (Hymenoptera: Formicidae) in the Iberá Nature Reserve, the Largest Wetland of Argentina LUIS A. CALCATERRA,1,2 FABIANA CUEZZO,3 SONIA M. CABRERA,1 AND JUAN A. BRIANO1 Ann. Entomol. Soc. Am. 103(1): 71Ð83 (2010) ABSTRACT The Iberá Nature Reserve in northeastern Argentina protects one of the largest freshwater wetlands and reservoirs of species in South America. However, key invertebrate groups such as the ants (Hymenoptera: Formicidae) remain almost unknown. The main objective of this work was to study the ground ant diversity in four main habitats of Iberá: grasslands, savannas, forests, and ßoating islands. Pitfall traps were used to characterize ground foraging ant assemblages, compare ant diversity among environments, and establish habitat associations. We also used bait traps, manual collections, and Winkler and Berlese extractors on the ground, vegetation, and litter strata to increase the species inventory. In total, 94 species in 30 genera were captured, representing the highest number of species reported from a survey of a protected area of Argentina. The richest genus was Pheidole Westwood with 23 species including three species reported for the Þrst time in Argentina. The most common species was Solenopsis invicta Buren. Overall, the savanna was the richest and most diverse habitat with the highest number of exclusive species and functional groups. The grassland showed the highest number of rare species, but only half of the expected species were captured. The forest showed the lowest ant richness, diversity, and equitability, but one half of the species were exclusive to forest habitat. Generalized myrmicines were predominant and dominant in all habitats. Our Þndings indicate that habitat specialization could be an important factor determining the organization of ant assemblages in Iberá. The protection of each of these unique and threatened natural habitats of Argentina is needed to ensure the long-term preservation of their exclusive ant species. KEY WORDS biodiversity, biological conservation, faunal survey, community structure, functional groups The Iberá Nature Reserve (1,300,000 ha), located in north central Corrientes province, Argentina, protects one of the largest freshwater wetland and reservoirs of species in South America (Parera 2006), with varied natural environments including grasslands, savannas, forests, freshwater lagoons with ßoating islands (Neiff and Poi de Neiff 2006, Parera 2006) and areas for cattle, rice, and commercial forests (Parera 2006). Some of the environments (mainly grasslands) are temporarily ßooded or burned; consequently, water and Þre play fundamental roles in the functioning and structure of this ecosystem (Adis and Junk 2002, Parera 2006). This great variability in time and space has affected its biota, because species are obliged to develop adaptations to the changes, making Iberá one of the richest and most diverse macroecosystems in the world (Parera 2006, The Ramsar Convention on Wetlands 2008). The maintenance of species diversity in this type of natural anthropic landscape mosaic is a central challenge of conservation biology. Important wildlife 1 USDAÐARS, South American Biological Control Laboratory, Bolṍvar 1559 (B1686EFA) Hurlingham, Buenos Aires, Argentina. 2 Corresponding author, e-mail: [email protected] 3 CONICET-Instituto Superior de Entomologṍa (INSUE), Facultad de Ciencias Naturales e Instituto Museo Lillo, Miguel Lillo 205 (T4000JFE), San Miguel de Tucumán, Argentina. in terms of preservation includes the broad-snouted caiman (Caiman latirostris Daudin), the yellow anaconda (Eunectes notaeus Cope), the Neotropical otter (Lontra longicaudis Olfers), the maned wolf (Chrysocyon brachiurus), and the marsh deer (Blastoceros dichotomus Illiger) (Neiff and Poi de Neiff 2006, Parera 2006). Despite being a refuge for many natural communities, only a few groups such as mammals, birds, reptiles or plants have been surveyed, whereas key invertebrate groups such as ants (Hymenoptera: Formicidae) have been scarcely studied. Ants are important components of the majority of terrestrial ecosystems in terms of biomass and diversity, playing an essential role in their function (Hölldobler and Wilson 1990). They are also useful indicators in monitoring programs and natural areas restoration efforts because of their fast response to changes in habitat quality, their abundance and relatively easy sampling and identiÞcation (Brown 2000, Kaspari and Majer 2002, Andersen et al. 2002). Some parameters of their communities, such as richness, relative abundances, and functional composition, are related to the environment (Andersen 1997). The detection of native ant species that have been accidentally introduced to new regions or continents is also of interest because of their potential injurious 0013-8746/10/0071Ð0083$04.00/0 䉷 2010 Entomological Society of America 72 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA effects on new ecosystems. At least Þve species of ants are included in the worldÕs 100 worst invasive alien species, and 28% of the 17 land invertebrates listed are ants (Lowe et al. 2000). Only a few ant surveys have been conducted in the Iberá Nature Reserve (Arbino and Godoy 2003, Jiménez Peréz 2006), and these surveys provide limited information because most of the few species reported were identiÞed only to genus. A detailed study of the ant fauna of Iberá would therefore contribute to our knowledge of ant diversity in this region and could help inform future monitoring and management programs. The main objective of this work was to study ground ant diversity in four different ecosystems of the Iberá Nature Reserve to characterize ant assemblages in terms of richness, relative abundance, species composition, and functional composition, and to determine whether characteristic associations existed between various surface-active ant species and the different habitats. Information gained from this work was then used to evaluate whether certain habitats within the Iberá Nature Reserve might be most valuable for conservation. Materials and Methods Study Area. The study was conducted from February 2007 to September 2008 in an area of ⬇140 km2 in the Iberá Nature Reserve (28⬚ 24⬘S, 57⬚ 14⬘W), Corrientes, Argentina, in four main natural habitats: 1) savanna (Espinal), dry woodlands or isolated trees and grasslands in the highlands; 2) grassland (Campos y Malezales), grassland surrounded by streams temporarily ßooded; 3) forest or gallery forest (Selva Paranaense), narrow humid forests, moderately modiÞed that borders the streams that drain both the savanna and the grassland; and ßow toward the marshes and rivers; and 4) ßoating islands (Esteros de Iberá), islands of ßoating vegetation, including bushes and small trees, in the Iberá lagoon (Neiff and Poi de Neiff 2006, Parera 2006). In total, 33 sampling stations were established as follows: 11 in savanna; eight in grassland; 11 in forest; and three in ßoating islands. The savanna and grassland stations were located in a private ranch (Rincón del Socorro, owned by the Conservation Land Trust Argentina S.A.) with ⬎5 yr of cattle exclusion. Forest stations were established in three locations: a 1.5-km2 fragment of gallery forest in Rincón del Socorro and in two 0.25-km2 fragments, 100 m apart, next to the Iberá lagoon and 25 km away from the larger fragment. The extension of the habitats in Rincón del Socorro were as follows: grassland, 6,032 ha; savanna, 4,992 ha; and forest, 562 ha. In a preliminary survey of the habitats (Maturo et al. 2007), an average of 29 ⫾ 8 plant species per station was recorded for the savanna and 21 ⫾ 4 plant species for grasslands. Island stations were set up opportunistically in the Iberá lagoon. The stations were located 1Ð2 km apart, except in the forest, where they were ⬇100 m apart, and located ⬎500 m from habitat limits or roads to avoid border effect (ecotones), except in the Vol. 103, no. 1 forest where they were placed ⬎30 m away. Stations were mapped using a GPS (Etrex model, Garmin). The climate is subtropical with a dry season in the winter (JuneÐSeptember), but with frequent summer droughts. Mean temperature varies from 15⬚C in July to 26⬚C in January. Mean annual rainfall is 1,500 mm, falling predominantly in the warm season (SeptemberÐMarch) (De Fina 1992, Fontan and Sierra 2004). Survey Methods. A combination of pitfall traps, baits, mini-Winkler and Berlese extractors, and manual collections were used to survey the ant fauna. Pitfall Traps. Unbaited pitfall traps are recommended for this type of study (King and Porter 2005). They were used to 1) characterize ground foraging ant assemblages, 2) compare ant diversity among environments, and 3) establish habitat associations. At each station, Þve pitfall traps (sampling unit) were set out every 10 m along a linear transect and exposed for 48 h. Each trap consisted of a 50-ml plastic centrifuge tube (⬇3 cm in diameter) buried in the ground and half-Þlled with soapy water. To minimize soil disturbance, pitfall traps were set up using a metallic tube to remove a soil plug exactly the size of the trap. After 48 h, the contents of the traps were removed, rinsed with water, and preserved in 96% ethanol. Most stations were sampled twice, except those in temporarily (several grassland stations) or permanently (all stations in the islands) ßooded areas. Resampled sites were located at least 10 m apart from the original site to maintain independence among samples. Thus, in total 56 sampling units (280 pitfalls traps) from 33 stations were obtained from the four habitats (Table 1). Although habitats were not sampled regularly during the seasons, the sampling was reasonably balanced between dryÐ cold (AprilÐSeptember) and rainyÐ warm (OctoberÐMarch) periods; an exception to this were the islands. Bait Traps. Sampling with baits was conducted in the savanna, grassland, and forest habitats to increase the inventory of species and the number of specimens captured of a given species to facilitate their identiÞcation, and to identify behaviorally dominant species. In total 220 baits were exposed in the proximity of the 22 pitfall stations as follows: eight in February, 10 in June, and four in November. At each station, 10 glass tubes (9 by 1 cm) containing a small piece of sausage in the bottom were placed every 10 m on the ground and exposed for 30 min, and then the tubes were picked up and plugged with cotton to avoid the escape of trapped individuals. The contents of the tubes were removed, washed, and the ants preserved in 96% ethanol for identiÞcation. Winkler–Berlese Extractors. Mini-Winkler and Berlese funnels were used in the forest to include ants of the leaf litter and to compare ant assemblages in the two gallery forest areas located 25 km apart. This sampling method was not used in other habitats because of the scarcity of the leaf litter stratum. In total, six 1-m2 plots were established in September 2007 and other six in September 2008, in the proximity of the pitfall sites. Plots were located ⬎50 m apart. The leaf litter (leaf mold, rotten wood) of each plot was col- January 2010 Table 1. CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ 73 Sampling effort in the four habitats in Iberá Date (season), sampling method Feb. 2007 (summer) Pitfall traps Baits June 2007 (fallÐwinter) Pitfall traps Baits Sept. 2007 (winterÐspring) Pitfall traps Winklers Nov. 2007 (spring) Pitfall traps Baits Sept. 2008 (winterÐspring) Berleses Total No. sampling units (no. pitfall traps, baits or 1-m2 litter samples) ⫹Savanna Grassland 6 (30) 6 (60) 2 (10) 2 (20) 8 (40) 8 (80) 5 (25) 5 (50) 5 (25) 5 (50) 10 (50) 10 (100) Forest 11 (55) 2 (12) 10 (50) 5 (25) 32 (215) 19 (130) lected up to 7 cm in depth. The 12 leaf-litter samples from 2007 were sifted (1 cm grid size) and put in mini-Winkler sacks. The 12 leaf-litter samples from 2008 were placed directly in Berlese funnels. Samples were extracted for 48 h and ants were separated from other arthropods and identiÞed to species or morphospecies by L.A.C. and F.C. under a dissecting scope. Voucher specimens were deposited at the Instituto Miguel Lillo, Tucumán, Argentina, and at the South American Biological Control Laboratory. Manual Collection. Opportunistic hand collections were made when possible to improve the ant inventory and include ants that forage on the vegetation stratum. Data Analysis. The number of ant species were recorded at the sampling unit level (Þve pitfall traps pooled), at the landscape level (pooling sampling units) for each habitat and grouping all habitats (regional scale). Species relative abundance was measured at the landscape level (by environment and grouping all habitats) as the proportion of sample units with each species because, for any given species, the number of ant workers is highly variable (Longino 2000). PresenceÐabsence data permit comparisons among different sampling methods (King and Porter 2005). Mean species richness per sample unit (square root ⫹ 0.5 transformation) were compared among habitats using one-way analysis of variance (ANOVA). Mean number of species and workers (square root ⫹ 0.5 transformations) extracted from Winklers and Berlese apparatus were compared among fragments of gallery forest by using a two-way ANOVA. Species richness was analyzed with EstimateS 8.0 software (Colwell 2006) by using presenceÐabsence data. Sample-based species accumulation curves were used to compare density of species (number of species per sampling unit) among environments (Gotelli and Colwell 2001) and as a tool to evaluate sampling efÞcacy (inventory completeness). Curves were obtained after 100 randomizations. A parametric (MMMeans) and two nonparametric indexes (ICE and Jack2) were used to estimate the total number of species expected to occur in each environment and Islands 3 (15) 9 (45) 4 (40) 2 (12) 28 (164) Total 14 (70) 2 (12) 24 (120) 4 (40) 3 (15) 2 (12) 82 (524) region (pool of available species). The Shannon (H⬘), Simpson (D), and Equitability (J) diversity indices (Magurran 1988) were used as additional estimators of diversity. Indexes were calculated using species relative abundance data with the statistical package Past version 1.82 (Ryan et al. 1995). Nonmetric multidimensional scaling based on a BrayÐCurtis dissimilarity matrix with presenceÐabsence data were used to compare similarity patterns among sampling units of each environment as determined by the composition of their ant assemblages. The Sorensen quantitative index was used to evaluate the similarity between the habitats (Magurran 1988). An analysis of indicator species was carried out using the indicator value method of Dufrene and Legendre (1997). This method identiÞes with an index the species that characterize a habitat. The index reaches its maximum (100%) when all individuals of a species are found in a single habitat type and when the species occurs in all sites (or sampling units) of that habitat. The signiÞcance of the indicator value for each species was evaluated using a Monte Carlo randomization test (900 iterations and signiÞcance level ⫽ 0.01). Only species that occurred in four or more sampling units were analyzed. These analyses were performed using PC-ORD 4.0 software (McCune and Mefford 1999). Functional composition was compared among habitats by assigning species to functional groups based on habitat requirement, competitive interactions, and global response of their species groups to environmental stress and disturbance (Bestelmeyer and Wiens 1996, Andersen 1997, Andersen et al. 2007, van Ingen et al. 2008). We followed the classiÞcation of functional groups proposed by Bestelmeyer and Wiens (1996) for Argentinean Chaco ants but including the Ecitoninae group (or army ants) within climate specialist group. Ant species were assigned to these groups based upon habitat and strata occurrence, presence, abundance, and observed behavior at baits, and previous work conducted mainly in South America on these and similar species with known natural history (Kusnezov 1978, Bestelmeyer and Wiens 1996, Andersen 1997, Silvestre et al. 2003, 74 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA 70 90% Exclusive 80% 50 Cumulative richness Number of species 100% Shared 60 Vol. 103, no. 1 40 30 20 10 0 Savanna Grassland Forest Islands Fig. 1. Total number of ant species (shared ⫹ exclusive) recorded pooling all methods in the four habitats surveyed in the Iberá Nature Reserve. Hcs 70% Ar 60% Sp At 50% Sc 40% Op 30% Cr 20% Gm 10% 0% S G F I Results Fig. 2. Functional group proÞles of the ants found in savanna (S), grassland (G), forest (F), and islands (I). Data are proportions of total species represented in each group: Op, opportunists; Sp, specialist predators; Sc, subordinate Camponotini; At, Attini; Cr, cryptics; Gm, generalized Myrmicinae; Ar, arboreals; Hcs, hot-climate species. Ant Diversity. In total, 94 ant species in 30 genera were found pooling records from the four collection methods (Appendix 1). Seventy six species (81%) were collected on the ground, 31 (33%) in the leaflitter, and 20 (21%) on the vegetation. The richest genera were Pheidole Westwood with 23 species, Camponotus Mayr, with 10 and Solenopsis Westwood with 7. The richest habitat was the savanna with 57 species (29 exclusive), and then the forest with 39 species (23 exclusive), the grassland with 29 (two exclusive), and Þnally the islands with 15 (seven exclusive) (Fig. 1). Only Camponotus ruﬁpes F. and Solenopsis sp. 3 inhabited all habitats, and only six species were sampled with all collecting methods (Appendix 1). Although the samplings were concentrated on the ground, at least one third of the species were recorded from at least two strata. Camponotus was the richest genus in the vegetation stratum (six species), whereas Pheidole was the richest both on the ground (22 species) and in the litter (six species). Eight functional groups were represented in the Iberá Nature Reserve: Opportunists, Specialist predators, Subordinate Camponotini, Attini, Cryptics, Generalized Myrmicinae, Arboreals, and hot-climate species. The highest number of species was found within the generalized Myrmicinae, with 25 species mainly in the genera Pheidole and Solenopsis; and then opportunists, with 15 species (Appendix 1). Functional composition varied among the different habitats (Fig. 2). Generalized Myrmicinae predominated in the grassland with 46.4% of the species, in the savanna with 35.2%, and codominated with cryptic species in the forest, with 27.8% of the species (Fig. 2). Arboreal species had the highest proportion in the island (26.7%). The second most common group was subordinate Camponotini in the savanna (18.5%) and islands (20%) together with arboreal species and generalized myrmicines. Opportunists were the second most common group in the grassland (17.9%) and forest (19.4%) together with Attini. Eight functional groups occurred in the savanna, seven shared with the grassland, plus the only four species recorded in the hot-climate specialist group (e.g., Pogonomyrmex cunicularius Mayr). Five functional groups were recorded in the forest and the islands (Fig. 2). Pitfall Traps. In total, 47 species (50% of the total species recorded in Iberá) were captured: 32 in the savanna, 22 in the grassland, 18 in the forest (Table 2), and seven in the islands. Ten species were only collected with this method. Accumulation curves of observed species were different among habitats (Fig. 3), with a higher accrual rate of species in the savanna. However, species accrual did not reach an asymptote in any of the environments, indicating that more species are expected to occur, especially in the grassland, where only 52% of the estimated terrestrial species were captured (Table 2) according to the richness estimator with the most stable asymptote (Jack2). The savanna also showed the highest mean number of species per sampling unit (Table 2), however signiÞcant differences were found only with the grassland (F2, 50 ⫽ 3.196, P ⫽ 0.049; TukeyÕs honestly signiÞcant difference test, P ⫽ 0.045). Although most differences in richness among ecosystems were not signiÞcant (P ⬎ 0.05), other diversity indicators (H⬘, D, and J) suggest that the savanna is more diverse (Table 2), showing more common species (10) than the other two habitats (six). Of the 47 species captured in pitfall traps, 19 (40.4%) were found in only one habitat. Approximately half of the ants captured in the forest (8/18) and the islands (3/7) were exclusives to these habitats. The most common ant was the red Þre ant, Solenopsis invicta Buren, captured in 41.5% (22/53) of the samples, very common in the savanna with the shortest herbaceous cover (66 cm in height) and well drained soil, common in the grassland with taller veg- Andersen et al. 2007, Calcaterra et al. 2008, van Ingen et al. 2008, Cuezzo and González Campero 2010). January 2010 Table 2. CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ 75 Diversity indicators of the three more intensely sampled habitats in Iberá No. Savanna (S) Grassland (G) Forest (F) S⫹G⫹F Stations Sampling unitsa Pitfall traps Expected speciesb Observed species (% of expected) Mean spp./sampling unit ⫾ SE Maximun spp./sampling unit Common speciesc Rare speciesd Exclusive speciese Invasive speciesf Indexes ShannonÐWiener (H⬘) Simpson (D) Equitability (J) 11 21 105 49 32 (65) 5.62 ⫾ 0.55 9 10 11 6 8 8 12 60 42 22 (52) 3.67 ⫾ 0.78 10 6 13 3 7 11 20 100 30 18 (60) 4.30 ⫾ 0.38 7 6 8 8 3 30 53 265 59 47 (80) 4.68 ⫾ 0.33 10 6 11 9 3.127 0.9415 0.9022 2.861 0.9298 0.9254 2.353 0.8734 0.8142 3.451 0.9584 0.8964 a Sampling unit consists of Þve pitfall traps buried in the ground and acting during 48 h. Estimated richness value with the most stable estimator (Jack2). Observed species in ⬎20% of the sampling units. d Observed species in only one sampling unit. e Observed species in only one habitat. f Invasive species or pest in Argentina (Lowe et al. 2000, Pest Directory 2008). b c etation (130 cm) and temporary ßoods, and absent in the forest and the islands. The ordination of the samples showed a clear separation between the forest and the other two terrestrial environments (Fig. 4). Similarity indexes were 54% for the savanna and grassland and only 10 and 5% between each one of them with the forest. Five species were associated with the forest (Table 3). Pheidole risii Forel was the most strongly associated with an indicator value of 85%, followed by Pheidole radoszkowskii Mayr (72.8%); P. risii was captured only in this habitat, and it was found in 85% of the samples. Three species were associated with the savanna, especially S. invicta (61.7%) followed by Pheidole aberrans Mayr (42.9%). S. invicta occurred in the 86% of the samples. Although with low indicator values, Paratrechina fulva (Mayr) (28.4%) and Pheidole sp. 3 (26.6%) were the only species associated with the grassland. Bait Traps. In total, 20 species were collected: 11 in the savanna, seven in the grassland, and four in the forest. The most common species trapped were S. invicta in the savanna (50% of the baits), P. fulva in the grassland (40%), and P. radoszkowskii in the forest (80%). Pheidole ﬂavens Roger, Ectatomma edentatum Roger, and Linepithema sp. were only collected with this method. Manual Collections. In total, 58 species were collected on the ground and/or vegetation stratum, 28 of which were collected only with this method such as the arboreal ant Nesomyrmex spininodis (Mayr). Winkler Collections. In total, 1,301 ants in 29 species were collected (Appendix 2), ranging from four to 116 individuals and from one to 12 species per m2. Ten species were only captured with this method (Appendix 1). The mean number of species per sample (Table 4) was similar between the two forest locations (F1, 20 ⫽ 0.673; P ⫽ 0.422) but not between extraction methods (F1, 20 ⫽ 7.40; P ⫽ 0.013). Interaction between location and method was not signiÞcant (F1, 20 ⫽ 0.908; P ⫽ 0.352). The mean number of workers was similar between locations (F1, 20 ⫽ 0.34; P ⫽ 0.566) and methods 2 1 Axis 2 Number of species 50 40 0 30 Savanna Grassland Forest S+G+F 20 10 -1 Savanna Grassland Forest -2 -2 0 -1 0 1 2 Axis 1 0 10 20 30 40 50 Number of sampling units Fig. 3. Species accumulation curves from pitfall trap data for individual habitats and regional (all samples pooled). Fig. 4. Nonmetric multidimensional scaling ordination plot from pitfall trap data showing differences in ant species composition among sampling units (points) located in different habitats (R2 ⫽ 0.75, stress ⫽ 0.21). 76 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Table 3. Vol. 103, no. 1 Ant species associated with habitat type from pitfall trap data No. sampling units with each sp. (%) Ant species Savanna n ⫽ 21 Grassland n ⫽ 12 Forest n ⫽ 20 Solenopsis invicta Pheidole radoszkowskii Pheidole risii Solenopsis sp. 4 Paratrechina fulva Pheidole sp. 3 Pheidole aberrans Wasmania auropunctata Paratrechina pubens Camponotus punctulatus cruentus 18 (86) 3 (14) 0 2 (10) 8 (38) 5 (24) 9 (43) 1 (5) 0 7 (33) 4 (40) 0 0 0 6 (60) 5 (50) 0 0 0 1 (10) 0 17 (85) 17 (85) 13 (65) 0 0 0 8 (40) 8 (40) 0 a b Indicator valuea (%) Habitat associationb 61.7 72.8 85.0 56.7 28.4 26.5 42.9 35.7 40.0 26.7 S F F F G G S F F S Maximum indicator value ⬎25% and P ⬍ 0.01. S, savanna; F, forest; G, grassland. (F1, 20 ⫽ 0.095; P ⫽ 0.761). Solenopsis sp. 4 and Wasmannia auropunctata (Roger) were common and numerically dominant with 561 and 289 workers captured, respectively, in 96 and 71% of the respective samples (Appendix 2). Moreover, the ant assemblages of both locations showed a similar species composition (Appendix 2). Approximately 26% of the species recorded in each location of gallery forest were exclusive, but uncommon (⬍20% occurrence in plots). Discussion Ant Diversity. This study, based on compositional and structural characteristics of the ant community, is one of the most exhaustive works conducted for a single region in Argentina. The number of species reported here (94) is, to our knowledge, the highest ever reported for a protected area in Argentina and doubled the number reported by Fuentes et al. (1998) for similar habitats and with similar collection methods in the smaller Otamendi Nature Reserve in Buenos Aires province (48 species). Also, it is 42% higher than the number of ant species reported by Leponce et al. (2004) for the Pilcomayo National Park in Formosa (66 species), although they sampled only forests with mini-Winkler extractors with a larger sampling effort. It is almost seven times higher than the species richness reported by Claver and Fowler (1993) for the Ñacuñán Biosphere Reserve in the Monte phytogeographical province (desert biome; Cabrera and Willink 1980) in Mendoza (14 species). The highest species richness reported for a nonprotected and Table 4. disturbed area in Argentina was reported by Bestelmeyer and Wiens (1996) for a grazing agroecosystem in the Chaco phytogeographical province (semiarid biome) in Salta province (104 species). The high species richness recorded in this work was the consequence of the variety of ecoregions and/or phytogeographical provinces that converge in the Iberá Nature Reserve (Kusnezov 1978, Cabrera and Willink 1980, Neiff and Poi de Neiff 2006). However, the number of species represents only 6% of the total estimated richness for Argentina and 14% of the 661 species identiÞed for this country (Cuezzo 1998). Our Þeld effort combined with literature information indicates that at least 105 species occur in Iberá. This number is 5 times greater than the 22 species reported by Arbino and Godoy (2003), although their study had other objectives. Thirteen species reported for Iberá by Arbino and Godoy (2003) and Jiménez Peréz (2006) were not found in our study, among these, the Argentine ant, Linepithema humile (Mayr). This was particularly unexpected because this invasive ant is highly associated with water bodies both in its native and introduced range (Ferster and Prusak 1994; Suarez et al. 2001; L.A.C., unpublished data). The expected number of epigeous ants for the pooled three most intensively sampled habitats was not much higher than the number actually observed (Table 2; Fig. 3). This difference was higher for the grassland, the less intensively surveyed habitat. The proportion of unique species per sampling unit, or singletons, for the grassland was 59%, which suggests that additional species should be found. Sampling Species richness and abundance of leaf-litter ants in two forest locations No. workers extracted (% in samples) No. Samplesa Species Mean species ⫾ SE Total workers Mean workers ⫾ SE a Iberá lagoon Rincón del Socorro Winkler (W) Berlese (B) W⫹B Winkler Berlese W⫹B 6 18 8.5 ⫾ 0.8 281 46.8 ⫾ 13.2 6 14 4.8 ⫾ 0.7 317 52.8 ⫾ 8.8 12 23 6.7 ⫾ 0.8 598 49.8 ⫾ 7.6 6 19 8.3 ⫾ 0.8 397 66.2 ⫾ 14 6 17 6.8 ⫾ 1.3 306 51 ⫾ 11.4 12 23 7.6 ⫾ 0.8 703 58.6 ⫾ 8.9 Each sample consists of leaf-litter collected from 1-m2 plot. Total 24 29 7.1 ⫾ 0.5 1,301 54.2 ⫾ 5.8 January 2010 CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ methods were complementary because 52 species (55% of total species) were exclusively collected with only one of the methods (Appendix 1). All species reported here are probably native from Argentina; however, this is the Þrst local record of Pheidole alpinensis Forel, Pheidole bison Wilson, and Pheidole nitella Wilson, previously known only from Brazil and Bolivia (Wilson 2003). The lack of exotic species could be the consequence of the geographical isolation of Iberá, being away from main highways and potential ports of entry of foreign species. In contrast, Ferster and Prusak (1994) reported that 35% of the ant species were exotic in the much less isolated subtropical wetland ecosystem of the Everglades National Park in Florida. It is possible, however, that foreign species occur in highly disturbed areas, such as grazed and cultivated Þelds and rural household landscapes of the Iberá region. Eleven species reported for Iberá (this work, Arbino and Godoy 2003) are considered exotic invasive pests in other countries (Appendix 1, Lowe et al. 2000, Pest Directory 2008), the most abundant of which was S. invicta. Functional Groups. The functional composition of ants in Iberá partially agreed with the model developed for arid-adapted ants in Australia (Greenslade 1978), later validated for other biomes in Australia and the United States (Andersen 1995, 1997; King et al. 1998). As in Chaco (Bestelmeyer and Wiens 1996), behaviorally dominant species (aggressive) of the subfamily Dolichoderinae (such as Iridomyrmex Mayr and Oecophylla Smith), common in Australia (Andersen 1997, Andersen et al. 2007, van Ingen et al. 2008), were absent, whereas climate specialists were scarce. As in North America (Andersen 1997, King et al. 1998), generalized Myrmicinae, such as the wide ranging species S. invicta, seems to be the ecologically equivalent group to the Australian dominant Dolichoderinae species; however, no equivalent to the fungus-growing ants of the Myrmycinae (tribe Attini) or Attini group seems to exist in Australia. Fire ants and other dominant Solenopsis species were included, following Bestelmeyer and Wiens (1996) and Hill et al. (2008), within Generalized Myrmicinae. The Australian climate specialist groups were poorly represented in Iberá. Only four of 94 species were assigned to the hot-climate specialist group in this study. This is consistent with Bestelmeyer and Wiens (1996), who assigned Forelius nigriventris Forel as the only climate specialist species (a hot-climate specialist speciÞcally) among the 104 species found in the Argentinean Chaco. These intercontinental differences suggest that a reclassiÞcation of the functional groups is necessary to generalize the model to other regions. The ant species composition of Iberá was closer to the South American functional groups (Bestelmeyer and Wiens 1996) or guilds (Silvestre et al. 2003, Cuezzo and González Campero 2010) than to the Australian groups (Andersen 1997, King et al. 1998), with the highest proportion of the ant fauna within the Generalized Myrmicinae group. The main difference with Bestelmeyer and Wiens (1996) was the absence of Ecitoninae species (army ants) in Iberá and sec- 77 ondly, the lower number of species of the subfamilies Dolichoderinae and Ponerinae. The absence of army ants included by Andersen (1997) in the Tropicalclimate specialist group was unexpected, because species of Neivamyrmex Emery occur at lower latitudes such as Buenos Aires (Kusnezov 1978). It is important to mention that the absence of species that only forage on the forest vegetation (arboreals) is mostly due to an insufÞcient sampling effort, because we did not sample the canopy, the forest highest stratum. Similarly, the absence of cryptic species in the islands was probably due to the permanent ßooded condition of this habitat. Species in Ectatomminae subfamily including Specialist predators as the millipede hunting Gnamptogenys tringularis (Mayr) and the large opportunistic species in genera Ectatomma and Odontomachus occurred mostly in the savanna, whereas in Ponerinae subfamily (cryptic and opportunistic species) occurred in the forest (Appendix 1). Ant Diversity Comparisons Among Habitats. Savanna Versus Grassland. Functional composition was similar in both habitats, except the absence of hotclimate specialists in the grassland (Fig. 2). The savanna was slightly richer in ant species than the grassland (Table 2), but this was uncorrelated with the higher number of plant species (r ⫽ 0.127, P ⫽ 0.727) or with the shorter grass coverage (r ⫽ ⫺0.39, P ⫽ 0.266) in the savanna (Maturo et al. 2007). According to the productivity hypothesis (Currie 1991), the energy entrance rate to a system limits the species richness by limiting the density of its individuals. For ants in particular, Kaspari et al. (2000) found that richness at the habitat level increased with density (nest/m2) and, primarily, with aboveground productivity. The savanna in Iberá showed 3 times more individuals and twice more ant biomass than the grassland (unpublished data), which would explain the higher richness found in the savanna as an indirect consequence of the apparent higher productivity of this habitat. However, a high net primary productivity is not the only cause of high ant diversity in the New World (Kaspari et al. 2000); habitat heterogeneity and moisture are other important components. Thus, the higher richness of the savanna could be explained by the greater vegetation variety of the savanna, where trees and shrubs are present in addition to grasses of similar structure and species composition to those of the grasslands (Maturo et al. 2007). The similarity in grass vegetation structure probably accounts for the relatively high habitat similarity index (54% similarity) for savanna and grassland, and the strong overlap of sampling units in the ordination plot (Fig. 4). Approximately 80% of the total grassland ant species also occurred in the savanna, probably in stations with higher grass coverage. However, the low number of exclusive species in the grassland, and consequently its lower richness, also could be the result of the low sampling effort. A better approach for future studies would be to consider two sub-habitats in the savanna according to the type of vegetation coverage (grasses and shrubsÐ trees). 78 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Savanna Versus Forest. Savanna showed twice as many species and three times more functional groups than the forest (arboreals, hot-climate specialists, and predator specialists), resulting in a no overlap in the ordination plot (Fig. 4) and low (10%) habitat similarity. Only 19% of the total species in the savanna also occurred in the forest. This is consistent with the fact that some species are open area specialists whereas others are forest dweller specialists (Hölldobler and Wilson 1990). However, the Neotropical forest-associated ant fauna is believed to be the origin of much of the Neotropical savanna fauna (Andersen et al. 2007, Ribas and Schoereder 2007). The question is what differs between these two types of habitats to make them have different species richness and composition? The higher richness of the savanna agrees with the trend found in Australia (Andersen et al. 2007, van Ingen et al. 2008) but not with that observed by Vasconcelos and Vihena (2006) in the Brazilian Amazon rain forest with twice as many aboveground ant species as the nearby savanna. The lower richness of the forest could be the consequence of the smaller area of this fragmented habitat (10 times less than the savanna) and the less and heterogeneous vegetation in the Iberá gallery forest compared with the Amazon primary forest. For example, the canopy ant fauna decreases in richness from tropical to subtropical forests, where it tends to be much lower than the ground fauna (Longino and Colwell 1997). Ribas and Schoereder (2007) and Correa et al. (2006) reported that species richness of the gallery forest in the Brazilian Pantanal increased with vegetation complexity and heterogeneity. In other studies conducted in the Brazilian Atlantic forest (Silva et al. 2007) and Cerrado (Silva et al. 2004), species richness and composition were positively affected by tree density and/or structural heterogeneity of the vegetation. Despite the similar sampling effort in the savanna and the forest (21 versus 20 samples), the shorter distance among the forest stations could have also inßuenced the number of species trapped in this habitat (McArthur and Wilson 1967). In addition, the undersampling of arboreal and litter ants contributed even more to the low richness recorded in the forest. Grassland Versus Forest. As in Fisher and Robertson (2002) for Madagascar, these habitats showed a similar overall species richness (Fig. 1). In spite of the differences in functional composition, low habitat level similarity (10%) and no ordination overlap, ⬇41% of the total species recorded in the grassland also occurred in the forest. This relatively high species overlap was probably a consequence of undersampling. Accumulation curves (Fig. 3) and estimation of expected species (Table 2) from pitfall traps seems to indicate that the grassland is richer in ant species than the forest, possibly because the sampling method used may capture more species in open areas, perhaps due to the less complex foraging environment. Fisher and Robertson (2002) found a strong differentiation in the species composition of these two environments mainly attributed to the absence of trees Vol. 103, no. 1 in the grassland. However, this does not seem to be the explanation for Iberá, where more species exploring the vegetation (including the arboreals) were captured on the ground of the temporally ßooded grassland (Appendix 1). A possible reason for the absence of arboreal species in the low stratum of the forest is that they actually prefer to forage in the highest vegetation stratum, the canopy. The higher proportion of cryptic species in the forest would be explained by the fact that surveys with Winkler and Berlese extractors were not conducted in the litter stratum in the grasslands. As reported by Ward (2000), most cryptic species in the forest were collected from the litter. Numerical Dominance. The ants associated with a particular habitat (mostly those of the generalized Myrmicinae group) were numerically dominant both in pitfall and bait traps. This would suggest a good adaptation of these species to the natural habitat. S. invicta was clearly the dominant species in the savanna (Table 3), which is consistent with a smaller scale study conducted in two moderately disturbed habitats in Corrientes (Calcaterra et al. 2008), indicating that this invasive ant can dominate natural and modiÞed habitats in its native range, with no signiÞcant impact on ant diversity. This contrasts with observations in its introduced range where Þre ants are almost absent in natural habitats free of disturbance (Tschinkel 2006; King and Tschinkel 2006, 2008). Another invasive ant, the opportunist P. fulva, was the most common species in the temporarily ßooded grassland, followed by Pheidole sp. 3 (putative Pheidole cf. industa Santschi) and S. invicta. The abundance of S. invicta (40% of the traps) in grasslands with tall grasses (averaged 130 cm) was higher than expected for a species that needs sunlight for colony thermoregulation. However, it agrees with Lubettazzi and Tschinkel (2003), who frequently found S. invicta in high grasslands in north Florida. As in other studies (Ward 2000, Leponce et al. 2004, Vasconcelos and Vilhena 2006), the dominant species of the forest (ground and leaf-litter strata) also were generalized myrmicines. P. rissi, P. radoszkowskii, and Solenopsis sp. 4 were numerically codominants on the ground and Solenopsis sp. 4 monopolized most of the baits, whereas the invasive Wasmannia auropunctata (Forel) was found only in the leaf-litter. P. risii also is mentioned as arboreal, whereas P. radoszkowskii is noted to be a typical ant of dry, open, and disturbed habitats (Kuznezov 1978). In our study, however, P. radoszkowskii was strongly associated with a dry, moderately modiÞed and closed forest. Consistent with observations of Þre ants (S. invicta) in introduced (King and Tschinkel 2008) and native ranges (L.A.C., unpublished data), we did not Þnd Þre ants colonizing nondisturbed forests. Implications for Biodiversity Conservation. Studies in the New World have been biased toward areas of high species diversity in the tropic. This work contributes to the general knowledge of ant diversity in the more poorly studied subtropical region. Little information is available on most ant species of this region, in terms of whether they are endemic (range, January 2010 CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ restricted) or threatened. Although ants have been recently included in global biodiversity conservation planning, none of the 149 ant species (many parasitic ants) included since 1994 in the International Union for the Conservation of Nature and Natural Resources (IUCN) Red List of Threatened Species (95% listed as vulnerable; IUCN 2009) were recorded in Iberá. Therefore it is very difÞcult to establish priorities for habitat conservation based on these key ant species. Data obtained on local species richness (observed and expected), diversity, equitability, habitat Þdelity, and functional group composition of ants, however, could tentatively be used to rank the most valuable habitats for conservation, at least until a better understanding of the distributional range, biology, and nesting requirements of different ant species are obtained, such that a conservation status could be assigned to these ants. Although the savanna showed a lightly higher ant diversity, we did not Þnd strong evidence to consider this habitat more valuable than others in terms of conservation. To preserve the ant species of Iberá, the four habitats should be protected, mainly because one third of the species recorded were exclusive to one habitat. One-half of the species of the forest, savanna, and ßoating islands occurred only in these environments, whereas others were strongly associated to a single habitat. For example, P. radoszkowskii was restricted to the forest, P. aberrans to the savanna and the putative Pheidole cf. industa to the grassland. Uniqueness of ant faunas by habitat was also reßected by the lack of overlap between the forest and the savanna or grassland in the ordination analysis. The high level of habitat Þdelity suggests that habitat specialization could be an important factor determining the organization of ant communities and promote coexistence of a great number of species in Iberá. This idea is consistent with Andersen (1997), Fisher and Robertson (2002), Vasconcelos and Vilhena (2006), Sarty et al. (2006), Correa et al. (2006), Ribas and Schoereder (2007), and Silva et al. (2007). The protection of these unique and threatened natural ecosystems of Argentina is needed to ensure the longterm preservation of their ant species. In summary, we reported the highest number of ant species (94) for a single and protected area in Argentina; however, more species remained undiscovered and more sampling efforts should be invested especially in the canopy, leaf-litter, and subterranean strata. Pheidole was the most represented genus, including three species reported for the Þrst time Argentina, and the invasive S. invicta was the most abundant species. South American functional groups need in depth investigation to allow intercontinental comparisons. Also, our studies revealed that habitats in Iberá are similarly important in terms of conservations of ant species. Studies on the effect of the vegetation structure and complexity, grazing, Þre, and ßooding on ant diversity and functional relationships (food webs, species interaction) are in progress, from which a better understanding of the dynamics of this macroecosystem will emerge. 79 Acknowledgments We thank John Longino (The Evergreen State College), Sanford Porter (USDAÐARSÐCMAVE, Gainesville, FL), Javier Casenave (Facultad de Ciencias Exactas y NaturalesConsejo Nacional de Investigaciones CientṍÞcas y Técnicas [CONICET]), Mario Di Bitteti (Laboratorio de Investigaciones Ecológicas de las Yungas-CONICET), Ann Fraser, and two anonymous reviewers for the help to improve this manuscript. We are grateful for the logistic support provided by the staff at Rincón del Socorro, especially Ignacio Jiménez Pérez, SoÞa Heinonen, Sebastián Cirignoli, Alicia Delgado, Yamil Di Blanco, and Malena Srur. We thank Alicia Delgado and Yamil Di Blanco for the help during some samplings and the staff at Iberá for permitting us to work in the Reserve. Cooperation for this research was provided by The Conservation Land Trust Argentina and CONICET. References Cited Adis, J., and W. J. Junk. 2002. Terrestrial invertebrates inhabiting lowland river ßoodplains of central Amazonian and central Europe: a review. Freshw. Biol. 47: 711Ð731. Andersen. 1995. A classiÞcation of Australian ant communities based on functional groups which parallel plant life-form in relation to stress and disturbance. J. Biogeogr. 22: 15Ð29. Andersen, A. N. 1997. Functional groups and patterns of organization in North American ant communities: a comparison with Australia. J. Biogeogr. 24: 433Ð 460. Andersen, A. N., L. T. van Ingen, and R. I. Campos. 2007. Contrasting rainforest and savanna ant faunas in monsoonal northern Australia: a rainforest patch in a tropical savanna landscape. Aust. J. Zool. 55: 363Ð369. Andersen, A. N., B. D. Hoffman, W. J. Muller, and A. D. Grifﬁths. 2002. Using ants as bioindicators in land management: simplifying assessment of ant community responses. J. Appl. Ecol. 39: 8 Ð17. Arbino, M. O., and M. C. Godoy. 2003. Formṍcidos (Hymenoptera) asociados a termiteros en el macrosistema del Iberá, pp. 55Ð74. In B. B. Alvarez [ed.], Fauna del Iberá. EUDENE. Corrientes, Argentina. Bestelmeyer, B. T., and J. Wiens. 1996. The effect of land use on the structure of ground-foraging ant communities in the Argentine Chaco. Ecol. Appl. 6: 1225Ð1240. Brown, W. L., Jr. 2000. Diversity of ants, pp. 45Ð79. In D. Agosti, J. D. Majer, L. E. Alonso, and T. R. Schultz [eds.], Standard methods for measuring and monitoring biodiversity, Smithsonian Institution Press, Washington, DC. Cabrera, A. L., and A. Willink. 1980. Biogeografṍa de América Latina (Serie de Biologṍa 13). Organización de los Estados Americanos, Washington, DC. Calcaterra, L. A., J. P. Livore, A. Delgado, and J. A. Briano. 2008. Ecological dominance of the red imported Þre ant, Solenopsis invicta, in its native range. Oecologia (Berl.) 156: 411Ð 421. Claver, S. H., and G. Fowler. 1993. The ant fauna (Hymenoptera, Formicidae) of the Ñacuñán Biosphere Reserve. Naturalia 18: 189 Ð193. Colwell, R. K. 2006. EstimatesS: statistical estimation of species richness and shared species from samples. Version 8.0 Persistent. (http://www.purl.oclc.org/estimates). Correa, M. M., W. F. Fernández, and I. R. Leal. 2006. Diversidad de formigas epigéicas (Hymenoptera: Formicidae) em Capões do Pantanal Sul Matogrossense: relações entre riqueza de especies e complexidade estructural da área. Neotrop. Entomol. 35: 724 Ð730. 80 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Cuezzo, F. 1998. Formicidae, pp. 452Ð 462. In J. J. Morrone and S. Coscarón [eds.], Biodiversidad de artrópodos argentinos. Ediciones Sur. La Plata, Argentina. Cuezzo, F., and C. González Campero. 2010. Invertebrados en la selva pedemontana Austral. El caso de Formicidae como ejemplo de caracterización de comunidades de insectos. In A. D. Brown, P. G. Blendinger, T. Lomáscolo, and P. Garcṍa Bes [eds.], Ecologṍa, historia natural y conservación de la Selva Pedemontana de las Yungas australes. Ediciones del Subtrópico. Tucumán, Argentina (in press). Currie, D. 1991. Energy and large scale patterns of animaland plant-species richness. Am. Nat. 137: 27Ð 49. De Fina, L. A. 1992. Aptitud agroclimática de la República Argentina. INTA, Academia Nacional de Agronomṍa y Veterinaria. Buenos Aires, Argentina. Dufrene, M., and P. Legendre. 1997. Species assemblages and indicator species: the need for a ßexible asymmetrical approach. Ecol. Monogr. 67: 345Ð366. Ferster, B., and Z. Prusak. 1994. A preliminary checklist of the ants (Hymenoptera: Formicidae) of Everglades National Park. Fla. Entomol. 77: 508 Ð512. Fisher, B. L., and H. G. Robertson. 2002. Comparison and origin of forest and grassland ant assemblages in the high plateau of Madagascar (Hymenoptera: Formicidae). Biotropica 34: 155Ð167. Fontan, R. F., and P. Sierra. 2004. Manejo y conservación de los Esteros del Iberá, módulo hidrologṍa. Proc. GEF/ PNUD/ECOS ARG/02/G35. Fuentes, M. B., F. C. Cuezzo, and O. R. Di Dorio. 1998. Ants (Hymenoptera: Formicidae) from the Natural Reserve of Otamendi, Buenos Aires, Argentina. G. It. Entomol. 9: 97Ð98. Gotelli, N., and R. K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4: 379 Ð391. Greenslade, P.J.M. 1978. Ants. The physical and biological features of Kunnoth Paddock in central Australia, pp. 109 Ð113. In W. A. Low [ed.], Technical paper no. 4. Division of Land Resources Management, Commonwealth ScientiÞc and Industrial Research Organization Division of Land Resources Management, Australia. Hill, J. C., K. S. Summerville, and R. L. Brown. 2008. Habitat associations of the ant species (Hymenoptera: Formicidae) in a heterogeneous Mississippi landscape. Environ. Entomol. 37: 453Ð 463. Hölldobler, B., and E. O. Wilson. 1990. The ants. Belknap Press of Harvard University Press, Cambridge, MA. [IUCN] International Union for the Conservation of Nature and Natural Resources. 2009. IUCN Red List of Threatened Species. Version 2009.1. (http://www.iucnredlist.org). Jiménez Pérez, I. 2006. Plan de recuperación del oso hormiguero gigante en los Esteros del Iberá. Corrientes, Argentina. (http://www.theconservationlandtrust.org). Kaspari, M., and J. D. Majer. 2002. Using ants to monitor environmental changes, pp. 89 Ð98. In D. Agosti, J. D. Majer, L. E. Alonso, and T. R. Schultz [eds.], Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, DC. Kaspari, M., S. O’Donnell, and J. R. Kercher. 2000. Energy, density, and constraints to species richness: ant assemblages along a productivity gradient. Am. Nat. 155: 280Ð293. King, J. R., and S. D. Porter. 2005. Evaluation of sampling methods and species richness estimator for ants in upland ecosystems in Florida. Environ. Entomol. 34: 1566 Ð1578. King, J. R., A. N. Andersen, and A. D. Cutter. 1998. Ants as bioindicators of habitat disturbance: validation of the Vol. 103, no. 1 functional group model for AustraliaÕs humid tropics. Biodivers. Conserv. 7: 1627Ð1638. King, J. R., and W. R. Tschinkel. 2006. Experimental evidence that the introduced Þre ant, Solenopsis invicta, does not competitively suppress co-occurring ants in a disturbed habitat. J. Anim. Ecol. 75: 1370 Ð1378. King, J. R., and W. R. Tschinkel. 2008. Experimental evidence that human impact drive Þre ant invasions and ecological change. Proc. Natl. Acad. Sci. U.S.A. 51: 20339 Ð 20343. Kusnezov, N. 1978. Hormigas argentinas: clave para su identiÞcación, Misc. 61, Fundación Miguel Lillo. Tucumán, Argentina. Leponce, M., L. Theunis, J.H.C. Delabie, and Y. Roisin. 2004. Scale dependence of diversity measures in a left-litter ant assemblage. Ecography 27: 253Ð267. Longino, J. T. 2000. What to do with the data?, pp. 186 Ð203. In D. Agosti, J. D. Majer, L. E. Alonso, and T. R. Schultz [eds.], Standard methods for measuring and monitoring biodiversity, Smithsonian Institution Press, Washington, DC. Longino, J. T., and R. K. Colwell. 1997. Biodiversity assessment using structured inventory: capturing the ant fauna of a tropical rain forest. Ecol. Appl. 7: 1263Ð1277. Lowe, S., M. Browne, S. Boudjelas, and M. De Poorter. 2000. 100 of the worldÕs worst invasive alien species. A selection from the Global Invasive Species Database, Invasive Species Specialist Group (ISSG) a specialist group of the Species. Survival Commission (SSC) of the World Conservation Union. (http://www.issg.org/pdf/publications/ worst㛭100/english㛭100㛭worst.pdf). Lubettazzi, D., and W. R. Tschinkel. 2003. Ant community changes across a ground vegetation gradient in north FloridaÕs longleaf pine ßatwoods. J. Insect Sci. 3: 21. Magurran, A. E. 1988. Ecological diversity and its measurement. Princeton University Press, Princeton, NJ. Maturo, H. M., L. J. Oakley, M. Scaraﬁocca, and D. E. Prado. 2007. Informe relevamiento de vegetación en estaciones de monitoreo. Estancia Rincón del Socorro, Corrientes, technical report. Universidad de Rosario, Santa Fe, Argentina. McCune, B., and M. J. Mefford. 1999. Multivariate analysis of ecological data version 4.01. MjM Software, Gleneden, Beach, OR. McArthur, R. H., and E. O. Wilson. 1967. The theory of island biogeography. Princeton University Press, Princeton, NJ. Neiff, J. J., and A. S. Poi de Neiff. 2006. Situación ambiental en la ecoregion Iberá, pp. 177Ð184. In A. Brown, U. Martṍnez Ortiz, M. Acerbi, and J. Corchera [eds.], La situación ambiental Argentina 2005, Fundación Vida Silvestre Argentina, Buenos Aires, Argentina. Parera, A. 2006. Un plan de manejo para la Reserva Natural del Iberá en la provincia de Corrientes, pp. 189 Ð194. In A. Brown, U. Martṍnez Ortiz, M. Acerbi, and J. Corchera [eds.], La situación ambiental Argentina 2005, Fundación Vida Silvestre Argentina. Buenos Aires, Argentina. Pest Directory. 2008. International Society for Pest Information. Griesheim, Germany. (CD format). Ribas, C. R., and J. H. Schoereder. 2007. Ant communities, environmental characteristics, and their implications for conservation in the Brazilian Pantanal. Biodivers. Conserv. 16: 1511Ð1520. Ryan, P. D., D.A.T. Harper, and J. S. Whaley. 1995. PALSTAT, statistics for palaeontologists. Chapman & Hall, London, United Kingdom. Sarty, M., K. L. Abbott, and P. J. Lester. 2006. Habitat complexity facilities coexistence in a tropical ant community. Oecologia (Berl.) 149: 465Ð 473. January 2010 CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ Silva, R. R., C.R.F. Brandao, and R. Silvestre. 2004. Similarity between Cerrado localities in central and southeastern Brazil based on the dry season bait visitors ant fauna. Stud. Neotrop. Fauna Environ. 39: 191Ð199. Silva, R. R., R. S. Machado Feitosa, and F. Eberhardt. 2007. Reduced ant diversity along a habitat regeneration gradient in the southern Brazilian Atlantic Forest. For. Ecol. Manag. 240: 61Ð 69. Silvestre, R., C.R.F. Brandão, and R. R. Da Silva. 2003. Grupos funcionales de hormigas: el caso de los gremios del Cerrado, pp. 113Ð148. In F. Fernández [ed.], Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia. Suarez, A. V., D. A. Holway, and T. J. Case. 2001. Predicting patterns of spread in biological invasions dominated by jump dispersal: insights from Argentine ants. Proc. Natl. Acad. Sci. U.S.A. 98: 1095Ð1100. The Ramsar Convention on Wetlands. 2008. The Ramsar list of wetlands of international importance. (http://www. ramsar.org). Appendix 1. group 81 Tschinkel, W. R. 2006. The Þre ants. Belknap, Harvard University Press, Cambridge, MA. van Ingen, L. T., R. I. Campos, and A. N. Andersen. 2008. Ant community structure along an extended rain forestsavanna gradient in tropical Australia. J. Trop. Ecol. 24: 445Ð 455. Vasconcelos, H. L., and J.M.S. Vilhena. 2006. Species turnover and vertical partitioning of ant assemblages in the Brazilian Amazon: a comparison of forests and savannas. Biotropica 38: 100 Ð106. Ward, P. S. 2000. Broad-scale patterns of diversity in leaflitter ant communities, pp. 99 Ð121. In D. Agosti, J. D. Majer, L. E. Alonso, and T. R. Schultz [eds.], Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, DC. Wilson, E. O. 2003. Pheidole in the New World: a dominant, hyperdiverse ant genus, Harvard University Press, Cambridge, MA. Received 13 May 2009; accepted 16 October 2009. List of the ant species found in the Iberá Nature Reserve and their collection method, stratum, habitat, and functional Subfamily, species Dolichoderinae Dorymyrmex steigeri platensis Santschi Dorymyrmex thoracicus Gallardo Forelius rufus Gallardo Linepithema micans (Forel) Linepithema sp. Ectatomminae Ectatomma edentatum Roger Gnamptogenys triangularis (Mayr) Gnamptogenys sp. Formicinae Brachymyrmex gaucho Santschi Brachymyrmex sp. 1 Brachymyrmex sp. 2 Brachymyrmex sp. 3 Brachymyrmex sp. 4 Camponotus blandus (Smith) Camponotus bonariensis Mayr Camponotus cameroni Forel Camponotus mus Roger Camponotus punctulatus cruentus Santschi Camponotus punctulatus punctulatus Mayr Camponotus ruﬁpes (F.) Camponotus substitutus Emery Camponotus sp. 1 Camponotus sp. 2 Camponotus sp. 3 Paratrechina docilis (Forel) Paratrechina fulva (Mayr) Paratrechina pubens (Forel) Paratrechina silvestrii (Emery) Myrmycinae Acromyrmex hispidus Santschi Acromyrmex lobicornis (Emery) Acromyrmex sp. 1 Acromyrmex sp. 2 Apterostigma pilosum Mayr Atta vollenweideri Forel Cephalotes depressus (Klug) Collecting methoda Stratum typeb Habitat typec Functional groupd P M P P B G G G G G S S S G F Hcs Hcs Hcs Op Op B P, M M G G G S S, G S Op Sp Sp M, E P, M M M M M P, M, B M P, M P, M, B P, M, B P, M, B M P M M P P, M, B P, M, E P, M, B, E G, L, V G V G G V G G G, V G, V G, V G, V G, V G G G G G G, L, V G, L, V I, F S, G S S S S S S S, G, F S, M S, G, I S, G, F, I S I S S G, F S, G F, I S, G, F Op Op Op Op Op Sc Sc Sc Sc* Sc Sc* Sc Sc Sc Sc Sc Op Op* Op* Op M P, M P, M M P, E P, M M G G G G G, L G V I S G, F I F S, G I At* At* At At At At* Ar Continued on following page 82 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Appendix 1. Vol. 103, no. 1 Continued Subfamily, species Cephalotes incertus (Emery) Cephalotes supercilii De Andrade Crematogaster quadriformis Roger Crematogaster sp. 1 Crematogaster sp. 2 Cyphomyrmex olitor Forel Cyphomyrmex rimosus (Spinola) Cyphomyrmex sp. Myrmicocrypta sp. Nesomyrmex spininodis (Mayr) Octostruma sp. Pheidole aberrans Mayr Pheidole alpinensis Forel Pheidole bergi Mayr Pheidole bison Wilson Pheidole dione Forel Pheidole ﬂavens Roger Pheidole gigaﬂavens Wilson Pheidole laevinota Forel Pheidole nitella Wilson Pheidole obscurifrons Santschi Pheidole obscurithorax Naves Pheidole radoszkowskii Mayr Pheidole risii Forel Pheidole rosula Wilson Pheidole rudigenis Emery Pheidole rugatula Santschi Pheidole spininodis Mayr Pheidole triconstricta Forel Pheidole vafra Santschi Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pogonomyrmex cunicularius Mayr Pyramica sp. Solenopsis globularia Creighton Solenopsis invicta Buren Solenopsis sp. 1 Solenopsis sp. 2 Solenopsis sp. 3 Solenopsis sp. 4 Solenopsis sp. 5 Strumigenys louisianae Roger Tetramorium sp. Trachymyrmex pruinosus (Emery) Trachymyrmex tucumanus (Forel) Trachymyrmex sp. Wasmannia auropunctata (Forel) Wasmannia sp. Ponerinae Hypoponera opaciceps (Mayr) Hypoponera sp. 1 Hypoponera sp. 2 Odontomachus chelifer (Latreille) Odontomachus haematodus (L.) Pachycondila striata Smith Proceratiinae Discothyrea neotropica Bruch Pseudomyrmecinae Pseudomyrmex pallidus (Smith) Pseudomyrmex phyllophilus (Smith) Collecting methoda Stratum typeb Habitat typec Functional groupd M M P, M, B M P, M P, E P, E P P, E M E P, M M M P M, B B M, E P, B M E P P, M, B, E P, B, M, E P P, M M P, M P, B, E M P, E E P, B M M E E P, M, B E P, M, B, E P, M, B, E P, E M P, E P, M P, E M E P, M, B, E E V V G G, V G, V G, L G, L G G, L V L G G G G G, V G G, L G G G, L G G, L G, L G G G G G, L G G, L L G G G L L G, V L G, L, V G, L G, L V G, L G G, L G L G, L, V L I S S, G S S, I F S, G, F S F S F S, G S S S, G, F S, I S F S, G S F S, G S, G, F F S, G S, G F S S, G, F S F F S, G S S F F S, G F S, F, I S, F, G, I F I G, F S, G F S F S, G, F F Ar Ar Gm Ar Ar At At* At At Ar Cr Gm Gm Gm Gm Gm Gm* Gm Gm Gm Gm Gm* Gm Gm Gm Gm Gm Gm Gm Gm Gm Cr Gm Gm Hcs Cr Cr Gm* Cr Gm Gm Cr Gm Cr Op At At At Gm* Cr P, E P, E E M P P, M G, L G, L L G G G G, F S, F F F I F Cr* Cr Cr Op Op Op E L F Cr P, M M G, V V G S Ar Ar Asterisk (*) refer to invasive and/or pest species. a P, pitfall trap; M, manual collection; B, bait trap; E, WinklerÐBerlese extractors. b G, ground; L, leaf-litter; V, vegetation. c S, savanna; G, grassland; F, forest; I, islands. d Op, opportunists; Sp, specialist predators; Sc, subordinate camponotini; At, Attini; Cr, Cryptics; Gm, generalized Myrmicinae; Ar, arboreals; Hcs, hot-climate species. January 2010 Appendix 2. CALCATERRA ET AL.: ANT DIVERSITY IN IBERÁ 83 List of leaf-litter ant species in two locations of gallery forest No. workers extracted (% in samplesa) Iberá lagoon Species Solenopsis sp. 4 Wasmannia auropunctata Brachymyrmex gaucho Pheidole radoszkowskii Strumigenys louisiane Solenopsis sp. 3 Hypoponera sp. 1 Paratrechina pubens Paratrechina silvestrii Hypoponera opaciceps Cyphomyrmex rimosus Pheidole risii Cyphomyrmex olitor Apterostigma pilosum Pheidole obscurifrons Hypoponera sp. 2 Pheidole gigaﬂavens Pheidole triconstricta Solenopsis globularia Solenopsis sp. 2 Pheidole sp. 2 Discothyrea neotropica Trachymyrmex sp. Pheidole sp. 1 Solenopsis sp. 1 Pyramica sp. Wasmannia sp. Myrmicocrypta sp. Octostruma sp. Total a Rincón del Socorro Winkler (W) Berlese (B) W⫹B Winkler Berlese W⫹B 95 (100) 93 (100) 18 (83) 5 (33) 3 (50) 3 (17) 5 (50) 5 (67) 0 0 10 (33) 0 1 (17) 9 (50) 5 (67) 17 (67) 0 1 (17) 3 (17) 0 3 (17) 1 (17) 0 3 (33) 0 1 (17) 0 0 0 281 222 (100) 44 (50) 5 (33) 9 (50) 0 9 (17) 17 (67) 0 1 (17) 0 0 3 (50) 1 (17) 1 (17) 0 0 0 1 (17) 0 0 2 (17) 0 0 0 0 0 0 1 (17) 1 (17) 317 317 (100) 137 (75) 23 (58) 14 (42) 3 (25) 12 (17) 22 (58) 5 (33) 1 (8) 0 10 (17) 3 (25) 2 (17) 10 (33) 5 (33) 17 (33) 0 2 (17) 3 (8) 0 5 (17) 1 (17) 0 3 (17) 0 1 (8) 0 1 (8) 1 (8) 598 101 (83) 138 (83) 34 (83) 16 (67) 25 (83) 12 (67) 0 7 (50) 30 (50) 6 (33) 3 (17) 2 (17) 1 (17) 0 3 (17) 0 4 (50) 0 2 (17) 5 (33) 0 0 3 (33) 0 4 (17) 0 1 (17) 0 0 397 143 (100) 14 (50) 22 (50) 3 (50) 12 (50) 39 (17) 3 (17) 2 (17) 14 (50) 19 (67) 8 (33) 10 (33) 6 (50) 5 (17) 0 0 2 (17) 1 (17) 0 0 0 3 (50) 0 0 0 0 0 0 0 306 244 (92) 152 (67) 56 (67) 19 (58) 37 (67) (50) 3 (8) 9 (33) 44 (50) 25 (50) 11 (25) 12 (25) 7 (33) 5 (8) 3 (8) 0 6 (33) 1 (8) 2 (8) 5 (8) 0 3 (25) 3 (17) 0 4 0 1 (8) 0 0 703 Total 561 (96) 289 (71) 79 (63) 33 (50) 40 (46) 63 (33) 25 (33) 14 (33) 45 (29) 25 (25) 21 (25) 15 (25) 9 (25) 15 (21) 8 (21) 17 (17) 6 (17) 3 (13) 5 (8) 5 (8) 5 (8) 4 (8) 3 (8) 3 (8) 4 (4) 1 (4) 1 (4) 1 (4) 1 (4) 1,301 Ants were extracted from a total of 24 samples of 1 m2: 12 per forest fragment (six samples using mini-Winklers and six with Berlese funnels).