Received 11 April 2016; accepted 4 June 2016; published 9 June 2016
Ants are one of the mega diverse insects that dwell at altitudes between 80˚N to 80˚S  ; they are found in all forest strata of terrestrial environments  -  . They live in society, so they are social, and occur in great diversity, richness and abundance  , acting at all trophic levels  . Studies in the canopy of tropical trees reported that over 50% of the arthropod fauna of the strata constituted of ants  -  . Surveys over the past 30 years, using new techniques for collecting, mainly in tropical areas, recorded a great abundance and diversity of new and unknown genera and species in tree canopies  -  , litter layer and soil  -  considerably expanding the bio ecological knowledge of the ant fauna that would serve as the basis for other studies.
In view of the above, a number of studies (bio ecological, behavioral, molecular, systematic, biogeographic, etc.) conducted globally have shown the important contribution of these animals in the dynamics of natural processes and standards, which value and recognize them as important environmental indicators. This helps to develop proposals for ecological-economic planning and wildlife management and conservation  -  .
Surveys of the ant fauna in the Brazilian Amazon, conducted primarily in biological reserves, the outskirts of large cities and in areas under environmental pressure, show that the taxonomic richness depends on the data collection methodology and habitat heterogeneity (Table 1). These studies do not confirm the theory that the richness and diversity increases towards east to west in the tropical areas.
Among the 110 genera of ants that dwell in Brazilian territory, 77 (70%) are rare, 31 (28.2%) are frequent, and 2 (1.2%) are abundant and have high species richness. On the other hand, 104 (80%) of the 110 genera known to Brazil dwell in the Brazilian Amazon, where 30 of them are represented by only one species; 54 of them by five or less and only one genus with more than 100 species (Table 2). This shows the need for increased collection efforts and other studies to better understand the dynamics of processes involving these communities.
However, the 21 genera, containing over 20 species, represent 69.08% (965 species) of species occurrence in Brazil, and only 11 of these, corresponding to 53.38% (560) of the species present and species richness similar in the Brazilian Amazon (Table 3). This shows the great gap in knowledge of this important group of insects in our area.
Today, science knows 13.188 ant species that belong to 16 subfamilies, 39 tribes, and 328 extant genera  . It is worth noting that from the 1980s, with the advent of new techniques for data collection, the number of species new to science increased noticeably, and these are being made available in the literature  -  . These studies are critical to know what exists and thus provide a basis for further research aiming to know the dynamics of patterns and processes developed by these insects in natural and disturbed environments.
Comparing the taxonomic richness of existing ants in the world, 27.64% (3646) of the species, 41.76% (137) of the genera and 81.25% (13) of the subfamilies dwell in the Neotropics; and, 10.59% (1397) of the species, 33.53% (110) of the genera and 81.25% (13) of the subfamilies are quoted in Brazilian territory     . On the other hand, 7.95% (1049) of the species, 31.70% (104) of the genera and 81.25% (13) subfamilies occur in the Brazilian Amazon (Table 4). This shows the need to broaden the knowledge of this group in Brazilian Amazonia.
Meanwhile, those results show that the large amount of ant fauna knowledge in Brazilian Amazonia came from biological stations. Then, the aim of this work is to see the “status of ant fauna at Caxiuanã National Forest (Ferreira Penna Scientific Station).
2. Material and Methods
This work is a compilation of ant publications and some collection from Caxiuanã National Forest      -  . The ants were collected in six plots delimited by Tropical Assessment and monitoring Initiative (TEAM/Caxiuanã) project. The ants were collected in leaf litter from 100 m divided in 10 samples away 10m apart. Each sample was taked in 1 m2 of leaf litter, sifted and transported to laboratory where was placed in mini-Winklers per 48 h  . All material was processed and identified at best taxonomic level in stereoscope Leica MZ12.5 by using keys and description of available literature  -  , and comparing with pictures from antweb, antwiki, and Invertebrate collection of Museum Paraense Emilio Goeldi. All results and published literature were compiled in EXCEL sheet. Appendix 1 is a dynamic table results in EXCELL program.
3. Results and Discussion
3.1. Status of Caxiuanã Ant Fauna
Although knowledge of the ant fauna in the Amazon has grown considerably in the last thirty years, little is known about their contribution to the bioecological process for balance and maintenance of the ecosystems in this biome.
It is known that, due to the large geographical area occupied by the Amazon, most research occurs in biological reserves, close to the major urban centers and areas designed for large environmental impacts, leaving many places with peculiar characteristics lacking information that would in some cases, direct proposals for the management and conservation of this biome (Table 1).
In this context, “Flona de Caxiuanã”, with rich and complex, often peculiar characteristics, is studied since the 1990s in several areas of scientific, technological and social knowledge. It has shown a tremendous physical and biological potential to base further research to provide an understanding of the processes that maintains the natural tropical system  -  .
Thus, the study of ants is being developed since the 1990s, approaching very interesting and important biological, ecological and taxonomic aspects to understand the patterns and processes that occur in these natural environments. Published and in development researches are detecting a great richness, diversity, and abundance in these communities composition, with the inclusion of several new species and over 30 new records at the genus level for this place, and others for the state of Pará and Brazil   -  .
3.2. Richness, Abundance and Composition of the Ant Fauna in Caxiuanã
In this study, we are including a list of 196 species belonging to 52 genera of 9 subfamilies of ants known for “Flona Caxiuanã” (Appendix 1). This richness is 5.40% of the species and 40.30% of the genera of the Neotropical Region; 14.10% and 53.36% of the species of the genera dwelling in Brazil, and 18.7% and 56.73% of the species of the genera of Amazon (Table 4).
Therefore, 21 of 52 genera are represented by three or more species, and concentrate 79.18% (156) of species (Appendix 1). However, 22 (37.29%) of the genera are represented by a single species. Otherwise, this richness is much lower than those quoted for the Ducke Reserve, in Manaus    and Catuaba Reserve in Acre  -  . It is noteworthy that only named species are on the list presented here, and there are undergoing studies to show a realistic scenario of bioecological aspects involving these insects to maintain the balance of this natural system  (Table 5).
Harada & Ketelhult  make an assessment on the quantification of regional ant fauna according to the capture methods and data analysis. They show that most of the results available in literature regarding Amazon are not comparable since it is a large variation between and within each method.
Moreover, Winkler collecting technique has a higher percentage of sampled specimens, including cryptic, rare, frequent and abundant species, even if it is timely and in a short time. It is believed that this happens because the sampled strata (leaflitter) are a complex mosaic and offer favorable resources (food and nesting) for the development of these insects. However, many species live in other strata (soil and vegetation) where they find all the necessities for their survival. In this context, as most collections made in Caxiuanã involved this substrate, it justify the fact that 153 (79.18%) of the 197 known species for the area have been collected using the Winkler technique, 66 (26%) of them using the pitfall methodology and 37 (18.78%) manually (Appendix 1).
Biological aspects of the ant fauna in Caxiuanã-considering the different sampling effort employed in collection techniques used in Caxiuanã no comparison was made in this regard. Species richness and some biological aspects of ant fauna in Caxiuanã are presented in Appendix 1. The subfamilies with larger numbers of genera and species were Myrmicinae (25 genera and 85 species), Ponerinae (12, 45), Formicinae (7, 12), Dolichoderinae (5, 09), Dorylinae (4, 13) and Ectatomminae (3, 25) (Appendix 1).
The predominance of species of the genus Crematogaster Lund, 1831 (12), Gnamptogenys Roger, 1863 (19), Neoponera Emery, 1901 (10) and Strumigenys Smith, 1860 (24) is due to ecological and taxonomic studies in the area involving these groups and the availability of taxonomic review in the literature. In this context, subfamily Ectatomminae (Ectatomma Smith, 1858, Gnamptogenys Roger, 1863 and Typhlomyrmex Mayr, 1862) was studied by Siqueira & Harada  , the genus Crematogaster Lund, 1831 by Felizardo & Harada  , Crematogaster Lund, 1831, Pachycondyla and Gnamptogenys by Souza et al.   , Odontomachus Latreille, 1804 by Bastos & Harada  , Dorylinae (Ecitonini) by Araújo & Overal  and Attini by Sanhudo et al.  . The genera Leptogenys Roger, 1861 was reviewed by Lattke  and Pachycondyla Smith, 1858 by Mackay  for the Neotropical region.
The ant fauna studied involves ants that live in leaf litter, soil and vegetation. Among the Ponerinae stands the Neoponera Emery, 1901 genus, which is distributed across the world. Most species are predators and build relatively simple nests in soil or litter, although some may nest in epiphytes and branches of plants in tropical areas. For example, Neoponera commutata (Roger, 1860), which is about 1.5 cm long, nests in soil, forages in small trails on the floor of primary forest, and, without showing great aggression, is predatory on termites (Syntermes modestus). Other species, such as Mayaponera (Mayr, 1884) and Pachycondyla harpax (Fabricius, 1804),
Table 1. Surveys of ant communities from various localities using different collection techniques in Amazonia region.
OBS: Bait (sardine, atum, honey); PAE-CM= Project of “Agroestrativista Chico Mendes”; R, Ducke= Reserve Ducke; PDBF = Program of Biological Dynamic in Forest Fragments, INPA/Smithsonian Institution, Veg.: vegetation.
Table 2. Level of abundance and species richness of the genera known from Brazilian Amazon.
OBS: rare < 10, Frequent = 10 to 100, Abundant > 100; lower richness < 10, high richness > 10; number of genera in parenthesis .
Table 3. List of genera with more species richness known from Brazil and Amazon, 2014.
Table 4. Ant richness comparison among areas (World, Neotropical region, Brazil, Amazônia) per taxonomic categories.
Table 5. Genera with more species richness in Caxiuanã, 2014.
are commonly found without much aggression, foraging in the leaf litter of the forest in the pristine Brazilian Amazon    , and little is known of their biology.
Ants of Ectatomminae subfamily can be found in wet and dry, pristine and/or disturbed forest, showing great flexibility of habits and habitats   . Generally, they are epigaeic, nest in soil or tree layers, and are opportunistic and generalist, having arthropods as their main food source   . Among the 24 species of this subfamily present in Caxiuanã, the most frequent and abundant in litter are Ectatomma edentatum (Roger, 1863), Ectatomma lugens Emery, 1894, Gnamptogenys horni (Santschi, 1929), Gnamptogenys relicta (Mann, 1916) and Gnamptogenys tortuolosa (Fr. Smith, 1858) that nest in soil, decaying wood or leaf litter, feed on animal and plant protein, and may forage in leaf litter from inside or outside the forest; E. edentatum (Roger, 1863), G. horni (Santschi, 1929), and, G. relicta (Mann, 1916) are easily collected with Winkler, However, E. lugens Emery, 1894and G. tortuolosa (Fr. Smith, 1858) are collected with pitfall and little is known of their biology  . Otherwise,, Ectatomma tuberculatum (Olivier, 1792) is found in edge and in the forest vegetation, usually feeding on extrafloral nectaries and/or homopterans at the apex of small shrubs.
The Dorylinae of the genera Eciton Latreille, 1804, Labidus Jurine, 1807, Neivamyrmex Borgmeier, 1940 and Nomamyrmex Borgmeier1936 that occur in the Neotropical region have nomadic and epigaeic habits, have fast movements and trail under or over leaf litter in forests, disturbed or not    -  The species Eciton burchelli (Westwood 1842), Eciton hamatum (Fabricius 1782) and Labidus praedator (Smith 1858) are very common and abundant in the Brazilian Amazon forests, and their diet consists of small invertebrates and vertebrates   . During their nest changings they form trails of several kilometers on the ground and on fallen logs, and carry small vertebrates (amphibians, small reptiles) and invertebrates that are in their path. They also are accompanied by small birds, monkeys and several groups of invertebrates that feed on (spiders, insects, invertebrates) and parasite (Diptera, Phoridae) groups of fauna found in these tracks  -  . In Caxiuanã, they were collected manually and in pitfall traps  .
Several species of the Myrmicinae subfamily are epigaeic, live in leaf litter of primary and secondary forest, and present omnivorous habits. From the 12 species of the genus Crematogaqster Lund, 1831, the most abundant species are Crematogaster brasiliensis Mayr 1878 Crematogaster carinata Mayr 1862, Crematogaster limata Fr. Smith 1858 and Crematogaster tenuicula Forel 1904, which present omnivorous habits, and forage in leaf litter. However, they can nest in trees, building carton and/or garden nests, except C. brasiliensis Mayr, 1878, which nests in hollow branches or decaying wood on the litter from tropical rainforests   . Others very common in leaf litter Myrmicinae species are Blepharidatta brasiliensis Wheeler, 1915, Octostruma balzani (Emery, 1894), Roger, Strumigenys elongate (Roger, 1863), Strumigenys perparva Brown 1958, Pheidole susannae Forel, 1886 and Wasmannia auropunctata (Roger, 1863), which live and forage in leaf litter.
Blepharidatta brasiliensis (Wheeler, 1915) are ancestors of attini, live in tropical rainforests where they nest among leaves litter or under wood fallen on the forest floor with populations between 20 to 200 individuals  . In Caxiuanã, they are very frequent and abundant in litter throughout the year, and are mentioned for the first time to this area.
Strumigenys perparva (Brown, 1958) and Strumigenys elongata (Roger, 1863) are very common and abundant in leaf litter of primary forest in Caxiuanã; they are voracious predators, have long jaws, jump to catch the prey, and, like most species of this genus, feed on small invertebrates; they dwell in South America, and S elongata (Roger, 1863) also occurs in Central America  -    .
Pheidole susannae Forel 1886 is very common and abundant in leaf litter of primary forest in Caxiuanã and in many places in South America, but little is known about its bioecology. Pheidole is one of the genera with worldwide distribution and one of the richest in number of species, with a wide range of habits and habitats  .
Some species are associated with myrmecophyte plants, like Pheidole minutula Mayr, 1878 which live in domatias of Maieta guianensis Aubl. in Central Amazonia and cultivate mealybugs  . Wasmannia auropunctata (Roger, 1863) is a common and abundant highly invasive species; it expels many native species in the tropical areas of the globe where it settles; considered a pest, it has omnivore habits, nests in soil and is highly aggressive  .
The Formicinae dwells from the tree canopy to the soil, nesting on the ground, in hollow stems and decomposing branches on the soil surface, in myrmecophyte plants domatias, plant hollows, building “ ant gardens”, “silk and carton nests” in forests and urban areas   ). The genus Camponotus Mayr, 1861 occurs throughout the world with 1098 species, over 400 of them occur in the Neotropics  ; the species in this genus have diversified habits and habitats and may be predatory, phytophagous and omnivorous; they nest from the tree crowns to the ground and branches and hollow, living or dead trunks, building “carton nests”, “silk nests”, “ants gardens”, etc. Camponotus femoratus (Fabricius, 1804), very aggressive, often making large trails on the ground and branches of plants, in wetlands and forest borde areas; building “ant gardens”, and, also, living in parabiosis with Crematogaster levior Longino, 2003  . Gigantiops destructor (Fabricius, 1804), a species of Neotropical distribution, with bizarre and large eyes that occupy almost the entire side of the head, is fast and shows no aggression; it nests in cavities in the soil, usually at base of Fabaceae plant. It forages more intensely from 9 to 11 am, looking for nectaries and small arthropods, reducing time and route taken in its territory, which reduces the risk of being preyed upon by lizards, spiders and mantises   . In Caxiuanã, it nests within the nest of Paraponera clavata (Fabricius, 1775), reason why is known by the natives as slave of bullet ant.
Most species of the Dolichoderinae subfamily live associated to plants, but are found in great abundance foraging in leaf litter and on the surface of soil in the Brazilian Amazon. Species of the genus Azteca Forel, 1878, occur in Neotropical region and some are distributed from southern Mexico to Argentina; they can nest in plants (myrmecophytes), or build “carton nests” or “ant gardens” in trunks or branches of trees and shrubs      . They are generally very aggressive, possess fast movements on or off tracks, raise the posterior region of the body (gaster) when in motion, and when disturbed, gather in large groups, releasing unpleasant odor to ward off the enemy  . The myrmecophyte species, such as Azteca alfari Emery, 1893, are distributed throughout the Neotropics, nest and feed on structures of plants of the genus Cecropia Loefling and are little aggressive     . On the other hand, the species of the genus Dolichoderus Lund, 1831 are, generally, over 5mm long, nest in trees, are little aggressive, move quickly, and can be found in all forest strata For example, Dolichoderus attelaboides (Fabricius, 1775) forages in apical branches and extrafloral nectaries at vegetation of forest edge, lacks aggressiveness and nests in hollow trees within the forest. However, Dolichoderus bidens (Linnaeus, 1758) move around quickly and aggressively, can be found in open areas, feeds on live seafood, extrafloral nectaries, other plant structures and other insects; builds “cardboard nests” on branches and leaves of a variety of plants, and can migrate according to their nutritional need. However, Dolichoderus bispinosus (Olivier, 1792) and Dolichoderus imitator Emery, 1894 are fast and often collected by the methodology of Winkler, in primary forest leaf litter; D. bispinosus (Olivier, 1792) nests in soil, moves in several long trails on the leaf litter and logs, fallen or not, in the forest, and very often is abundant also in sardine baits. Little is known of the biology of D. Imitator Emery, 1994.
Most species of the Pseudomyrmecinae subfamily have arboreal habits, nesting in domatias, trunks and hollow branches, fallen or not. Usually, they are predators, have an elongated body and move with great speed. Of the seven species recorded for “Flona Caxiuanã”, Pseudomyrmex tenuis (Fabricius, 1804) is very common in leaf litter and leaves of trees and shrubs, in shaded or sunny areas in the Brazilian Amazon; however, little is known about its biology. Also, Pseudomyrmex viduus (Smith, 1858), as all species that colonize domatias of plants of the genera Tachigali Juss. (Caesalpinaceae) Loelfling and Triplaris. ex L. (Polygonaceae) keep mealybugs (Coccodea) in the wall of domatias, releasing a sugary substance (“honeydew”), which is used by the ants as food. These ants are more aggressive than other species of the genus  . They can colonize other myrmecrophytes, such as those of the genera Cordia L., Coussapoa Aubl., Ocotea Aubl., Pseudobombax, Pterocarpus Jacq. and Sapium P. Browne   .
3.3. Final Considerations
Although the study of the ant fauna of “Flona Caxiuanã” has been going for about 20 years, current knowledge is very incipient, considering the richness and diversity of habits and habitats found there.
The general aspects of the richness, diversity and abundance of the ant community know are based in some collection methods on the leaf litter layer, where, it is believed that occur higher richness and abundance of these animals. More detailed studies of this fauna are in development and will significantly improve the current status. However, much needs to be done to stabilize the community structure of this important group of insects in order to increase the knowledge to better understand their contribution on the dynamics of physical and biological processes that maintain this natural system.
Likewise, the capacity of the human resources at various academic levels is an important means to accelerate the production of the knowledge, and thus meet this demand.
The high ant species richness and diversity of ant fauna from Caxiuanã National forest is because of its high habitats heterogeneous and conservation forests.
Many studies need to be done in this place to understand the ant community pattern to give base for other studies and proposal for use, management and conservation of this interesting Amazonia place.
I am grateful to Tropical Ecology Assessment and Monitoring Initiative Program for financial and logistic support.
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