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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).