Open-access Frontier ants (Hymenoptera: Formicidae) unveiled: exploring the remarkable diversity of the Brazilian Far West

Formigas fronteiriças (Hymenoptera: Formicidae) reveladas: explorando a notável diversidade do extremo oeste brasileiro

Abstract:

The Parque Nacional da Serra do Divisor (PNSD), renowned for its remarkable biodiversity, is a conservation unit of the Amazon biome situated at the westernmost limit of the Brazilian territory. However, the PNSD fauna is still poorly documented for most taxa. This study aimed to list the ant species (Hymenoptera: Formicidae) of the PNSD, comparing its diversity found with studies conducted in other hotspots of biodiversity of the world. Field collections were conducted in the northern region of PNSD for four days in 2016, using three collection methods: epigaeic pitfall traps, Winkler extractors, and hand collections. Even with the short sampling period, an impressive number of 261 species of ants were recorded, representing one of the highest richness documented for ants with the least sampling effort applied in a single locality worldwide. Of these species, 66 were newly recorded in the state of Acre, with six representing first-time records for Brazil. These findings highlight the critical importance of the PNSD as a strategic area for ant conservation, both in Brazil and globally.

Keywords: Amazon; ant richness; conservation units; Formicidae; inventory; Serra do Divisor

Resumo:

O Parque Nacional da Serra do Divisor (PNSD), conhecido por sua notável biodiversidade, é uma unidade de conservação do bioma Amazônico situado no limite mais ocidental do território brasileiro. Contudo, a fauna do PNSD ainda é pouco documentada para a maioria dos táxons. Este estudo teve como objetivo listar as espécies de formigas (Hymenoptera: Formicidae) do PNSD, comparando a diversidade encontrada com estudos realizados em outros hotspots de biodiversidade do mundo. As coletas de campo foram realizadas na região norte do PNSD durante quatro dias no ano de 2016, utilizando três métodos de coleta: armadilhas epigeicas de queda, extratores de Winkler e coletas manuais. Mesmo com o período curto de amostragem, um número impressionante de 261 espécies de formigas foi registrado, representando uma das maiores riquezas documentadas para formigas com o menor esforço amostral aplicado em uma única localidade em todo o mundo. Destas espécies, 66 são novos registros para o estado do Acre, dos quais seis são registros inéditos para o Brasil. Essas descobertas destacam a importância crítica do PNSD como área estratégica para a conservação das formigas, tanto no Brasil quanto no mundo.

Palavras-chave: Amazônia; riqueza de formigas; unidades de conservação; Formicidae; inventário; Serra do Divisor

Introduction

The Amazon Rainforest is known for its high diversity and its crucial role as carbon storage, which contributes to mitigating the consequences of global warming (Fearnside 2012, 2021, Marin et al. 2022). Nevertheless, the increase in deforestation rates in Brazilian Amazon over the past decade is a matter of concern among scientists due to the increasing biodiversity loss (Franco et al. 2019, Feng et al. 2021, Silva Junior et al. 2021, Portal TerraBrasilis - INPE 2024). To address this issue, one of the most effective strategies is to promote the establishment and ongoing maintenance of conservation units (Oliveira et al. 2021b, MMA 2023).

In Brazil there are 2,859 conservation units, which represents 19% of the country’s continental territory. The Parque Nacional da Serra do Divisor (PNSD) is a Conservation Unit situated in Acre state, on the western frontier of Brazil, encompassing an expanse of 8,284.51 km2 of well-preserved forest (MMA 2024). However, since the creation of the PNSD, in 1989, a road that would connect the interior of Acre to Peru has been planned to cross from one boundary of the park to the other (Federal Decree N° 97.839). This threat is added to a bill (No. 6024/2019) that is currently under consideration by the Brazilian government and provides for the change of category of the PNSD to an “Environmental Protection Area”, which would allow mineral exploration in the region (Ruaro & Laurance 2021, Koga et al. 2022).

If the threats suffered by the PNSD materialize, in addition to the social losses, the environmental damage could be irreversible, since the park is the only Brazilian conservation unit that covers the transition between the Amazon region and the Andes (Ruaro & Laurance 2021, Koga et al. 2022). Furthermore, although the scarce data on the biodiversity of the PNSD, it is known that the park is home to an enormous richness of animal and plant species (MMA 1998, Calouro 1999, Whitney et al. 2004, Morato et al. 2008, Koga et al. 2022). With the imminent threat of deforestation, surveys of local fauna and flora become even more urgent to advance knowledge about the richness of species in the western limit of Brazil.

Insects reign as the most diverse group of animals worldwide, with over a million described species (Stork 2018). Found in virtually all terrestrial ecosystems, they play crucial roles in ecosystem services such as pollination, herbivory, predation, and nutrient cycling (Noriega et al. 2018, Elizalde et al. 2020). However, in recent decades, several studies have warned about the rapid decrease in insect populations, raising discussions about the urgent need to develop strategies for their conservation (Habel et al. 2019, Forister et al. 2019, Wagner 2020).

Ants are known for their remarkable abundance and omnipresence in almost all terrestrial ecosystems of the planet (Schultheiss et al. 2022). Due to their high diversity and biomass, ants are essential for maintaining ecosystem functions such as predation, seed dispersal, and soil fertility (Wills & Landis 2018, Elizalde et al. 2020). Despite the recognized importance of these insects, knowledge about the conservation status of most species is still incipient. In the latest Red Book of Brazilian Fauna Threatened with Extinction, published in 2018, only 95 out of over 1500 ant species occurring in Brazil were included (ICMBio 2018, Feitosa et al. 2022). However, even among these 95 species, more than 20% (21 species) were not evaluated due to insufficient data (ICMBio 2018).

The PNSD is located in a region of Brazil considered a priority for ant collection due to the scarce sampling efforts in this region (Divieso et al. 2020, Schmidt et al. 2022). Studies in several animal groups have revealed the potential of the PNSD not only to document new species records for Brazil but also to discover new taxa (Azevedo & Batista 2002, Whitney et al. 2004, Dolibaina et al. 2015).

Conducting rapid inventories of local fauna is one of the most important strategies for species conservation, as it allows for the delimitation of endemic areas and mapping of species distributions (Samways et al. 2020). Therefore, the goal of this study was to list the ant species of the PNSD, both to reinforce the argument for the park’s biodiversity and the need for its preservation and to update information regarding ants occurrence and distribution in Brazil.

Material and Methods

1.

Study area

The Serra do Divisor National Park is located on the western edge of the state of Acre, Brazil, covering territories in the municipalities of Mâncio Lima and Cruzeiro do Sul, between the following coordinates: North: 07°07’00” S and 73°48’20” W; East: 09°08’40” S and 72°40’00” W; South: 09°24’40” S and 73°12’40” W; West: 07°32’40” S and 73°59’20” W (Federal Decree N° 97.839) (Figure 1). The climate of the region is classified as tropical without a dry season, characterized by the temperature of the coldest month not exceeding 18°C and rainfall of the driest month equal to or greater than 60 mm (Alvares et al. 2013). The predominant vegetation type is lowland tropical forest, although mosaics with a typical highland composition are also present. Collections were concentrated in the northern zone of the park, probably the area with the greatest biodiversity (MMA 1998).

Figure 1
Location of the Serra do Divisor National Park (PNSD). The black square inside the PNSD represents the area where ant sampling was conducted.
2.

Collection

Collections were conducted between November 15th and 18th, 2016, using epigaeic pitfalls, Winkler extractors and manual sampling. The pitfalls were installed on the 15th along the Formosa trail (7°26’17.19” S 73°39’27.39” W, 245 m) and were distributed along three transects, each 500 meters long and spaced 1 km apart from each other. Each transect had 20 pitfalls, consisting of 300 mL plastic cups with a 10 cm opening, containing a solution of water and detergent. Following a 48-hour exposure period, the pitfalls were retrieved, and the ants separated.

Winkler extractor collections (33 samples, 11 each day) were qualitative and involved sieving 1 m2 of leaf litter along with a small surface layer of soil. Each sieved sample was placed in a cloth bag and suspended in a Winkler extractor. A cup containing a moist damp flannel was attached to the bottom of each extractor. After three hours, the cups were removed, and their contents were emptied into a white tray to separate the live ants, which were transferred to vials containing absolute ethanol. This process was repeated after six hours and again after 24 hours. Both Winkler extractor and manual collections were conducted on November 16th, 17th, and 18th during the day along the three main trails within the PNSD: Formosa trail (7°26’17.19” S, 73°39’27.39” W 245 m); Mirante trail (7°26’56.65” S, 73°40’13.94” W, 345 m), and Barreiro trail (7°27’9.22” S 73°39’58.24” W 260 m). Manual sampling was also qualitative, involving active searches for ants both on the ground and in the vegetation in the intervals of Winkler extractor events in the three trails assessed. Hand collections were also carried out on the banks of the Moa River (7°26’58.81” S 73°39’37.83” W 245 m), which crosses the northern portion of the park.

3.

Identification

Ants were identified to genus level using Baccaro et al. (2015). For identification at species level, specific keys available for each genus were used: Gonçalves (1961); Kempf (1966); Watkins (1976); Mackay (1996); Lattke (1997); Bolton (2000); Fernández (2003); Longino (2003); Longino & Fernández (2007); Wild (2007); Arias-Penna (2008); Fernández (2008); Mackay & Mackay (2010); Pacheco & Mackay (2013); Ješovnik & Schultz (2017); Fernández & Guerrero (2019); Fernández & Serna (2019); Oliveira & Feitosa (2019); Ortiz-Sepulveda et al. (2019); Solomon et al. (2019); Ward (2019); Camacho et al. (2020); Chaul (2020); Ladino & Feitosa (2020); Longino & Branstetter (2020); Ulysséa & Brandão (2021); Fernandes et al. (2021); Oliveira et al. (2021a); Barrera et al. (2022); and Williams et al. (2022). For the genus Camponotus, which lacks a key for Brazilian species, we compared our morphospecies with images of type specimens on Antweb (https://www.antweb.org). Additionally, specialists were consulted for taxa currently under taxonomic study, namely Frederico Marcineiro (Pachycondyla); Eder França (Dolichoderus and Odontomachus); Paloma Andrade (Neocerapachys and Syscia); Jaqueline Paes (Nomamyrmex); Lívia Prado (Megalomyrmex and Octostruma); Otávio Silva (Rogeria); and Alexandre Casadei-Ferreira (Pheidole). All specimens were deposited at the Padre Jesus Santiago Moure entomological collection, Universidade Federal do Paraná, Curitiba, Brazil (DZUP).

4.

Literature revision

In order to compare the diversity found in this survey with previous studies in Brazil, we consulted Feitosa et al. (2022). Additionally, we also conducted a brief literature review to gather lists of ant species around the world. This involved searching in the Web of Science database the keywords “ants” and “list” in the Web of Science collection spanning all years. We then filtered the retrieved papers by removing the proceedings papers. In total, the abstracts of 775 works were analyzed (Supplementary material).

To verify possible new records of occurrence in the state of Acre or in Brazil, we compared the species found in the present study with lists of species from Acre previously published by Miranda et al. (2012) and Schmidt et al. (2020), as well as with the list of Brazilian species by Feitosa et al. (2022). Additionally, we consulted revision works for each genus (cited previously in the “Identification” section). Furthermore, we searched the antmaps.org database for species (Janicki et al. 2016, Guénard et al. 2017). For all records found on antmaps.org, we consulted the cited sources to ensure data accuracy.

5.

Data processing

The map illustrating the location of the park was generated using the QGIS 3.32 software. Three shapefile files were used in the construction of the maps: one for the delimitation of the countries of South America (ANA 2010), one to delimit the state of Acre (IBGE 2022) and finally another with the delimitation of the PNSD (ICMBio 2024).

Seven species (Figure 2) were photographed using the Zen 2.3 software and the Zeiss Stereo Discovery V20 stereomicroscope, equipped with the Zeiss Axiocam 305 color video camera. Images and boards were processed using GIMP 2.10.34.

Figure 2
Ants recorded in Brazil for the first time in the literature. A: Apterostigma callipygium; B: Linepithema piliferum; C: Pheidole cuevasi; D: Pheidole demeter; E: Pheidole gilva; F: Pheidole sanax. Images by the authors.

Results

A total of 261 species were collected distributed among 56 genera and 10 subfamilies. Among these, 171 were identified, five were indicated as near to known species (nr.) and 85 remained unidentified and were here considered as morphospecies. Notably, among the unidentified species, at least 23 are new to science, one of them being a new genus (Table 1) (Dias & Feitosa in prep., Silva et al. in prep., França et al. in prep., Feitosa et al. in prep.). The genera with the highest number of species were Pheidole (58), Hypoponera (15), Strumigenys (15), and Camponotus (14).

Table 1
List of species in the Parque Nacional da Serra do Divisor and their respective collection methods. W = Winkler extractor; M = Manual sampling; P = Pitfall traps. Species marked with “*” represent first records for Acre and “**” represent first records for Brazil.

The method that collected the greatest diversity was the pitfall sampling accounting for 138 species, followed by the Winkler extractor with 121 species, and hand collections with 75 species. Remarkably, the majority of species (198) were exclusively captured by a single method, with pitfall traps recording the highest number of exclusive species (85), followed by the Winkler extractor (74), and hand collections (39).

An impressive number of 66 species were recorded for the first time in the state of Acre, six of which were also the first records for Brazil: Apterostigma callipygium, Linepithema piliferum, Pheidole cuevasi, Pheidole demeter, Pheidole gilva and Pheidole sagax (Table 1, Figure 2).

Discussion

Based on the diversity uncovered in the present survey and considering the short period of sampling (four consecutive days) and the effort employed (three collection methods), it can be inferred that the PNSD is one of the places with the highest ant diversity in Brazil, and perhaps in the world. While previous surveys in Brazil have reported comparable or greater richness, it is notable that these studies typically involved significantly larger sampling efforts. For instance, Solar et al. (2016) documented 285 ant species across 18 areas within a territory spanning 2 million hectares in the eastern Amazon. Camacho & Vasconcelos (2015) registered 277 species in a single reserve in the Brazilian Cerrado, but the records are based in 10 years of samplings. Specifically for the state of Acre, western Amazon, a survey carried out by Oliveira et al. (2009) over three and a half years of collections recorded 276 ant species. Finally, an inventory carried out in Xapuri, also in Acre, by Miranda et al. (2017) recorded only two more species than our study (263 in their study, compared to 261 in ours), despite involving three collection events divided between three years using epigaeic pitfalls and vegetation beating method. The fact that two of the surveys with the highest species diversity were conducted in Acre suggests that this portion of the Brazilian Amazon may host one of the greatest ant diversities in the country.

The findings from the present study also stand out in a global context. Among the 775 studies analyzed, only two revealed a similar ant richness, albeit with considerably greater sampling efforts. In a study conducted in a protected area in Panama, Leponce et al. (2021) reported results from a year-long sampling effort combining 11 collection methods, which resulted in 405 species. Another study in Cameroon documented 306 species over a year and a half, using four collection methods: hand collecting, bait trap, Berlese extraction and pitfall traps (Tchoudjin et al. 2020). In light of this context, it is possible to place the PNSD in the global biodiversity spotlight, since the number of species recorded in the park over just four days distinguishes it as one of the surveys with the highest ant species richness documented ever.

More than 75% of species were exclusively captured by a single method, indicating that the combination of collection methods is the better approach to cover the highest ant diversity possible, as demonstrated by Delabie et al. (2021). The use of epigaeic pitfalls allows the capture of ants that walk on the soil surface, whereas the Winkler extractor is efficient for collecting ants that nest and forage in the interstices of the leaf-litter (Fisher 1999, Delabie et al. 2021). Since no traps were installed in the vegetation, manual collections were crucial for sampling some arboreal genera, such as Pseudomyrmex and Cephalotes, of which all species were collected manually.

The high diversity of Pheidole observed in this study is an expected result, as demonstrated by Feitosa et al. (2022), which showed that this is the most frequent genus recorded in ant diversity studies in Brazil. In fact, Pheidole stands as the most diverse ant genus in the world, boasting 1160 species and 124 subspecies described, with approximately 200 recorded in Brazil (Bolton 2024, AntWeb 2024). The large number of Strumigenys and Camponotus species recorded in the PNSD also corroborates Feitosa et al. (2022), who found these two genera (albeit with Camponotus preceding Strumigenys), to be the most specious after Pheidole. Camponotus ranks as the second most diverse genus worldwide, with 1086 species and 411 subspecies described, including approximately 170 occurring in Brazil (Bolton 2024, AntWeb 2024). Meanwhile, the richness of Strumigenys can be attributed to two factors: the high diversity of species (879, of which approximately 90 are recorded in Brazil) combined with the collection technique (Bolton 2024, AntWeb 2024). Among the 15 Strumigenys species found, 13 were captured exclusively using the Winkler extractor, underscoring the significance of this technique for collecting ants that nest and forage in leaf litter.

Hypoponera also stood out in our study by its great richness in the PNSD (15 species), which may be attributed to the use of the Winkler extractor, as these ants are among the most commonly found in the leaf-litter (Bolton & Fisher 2011). As demonstrated by Feitosa et al. (2022), Hypoponera is generally represented in studies by morphospecies, lacking specific-level identification, which is also the case in this study, with 13 out of the 15 species remaining unidentified. This issue stems from the dearth of taxonomic studies on the genus in Neotropical region, but an ongoing taxonomic revision by the authors of the present study has revealed that all 13 morphospecies listed here represent new species. Furthermore, new species were also recognized for six other genera (Table 1). This underscores the significance of the PNSD in advancing our understanding of ant diversity in Brazil.

Although our results are relevant from the point of view of the high richness of species recorded in a single conservation unit, the absence of frequently collected genera that have records in the state of Acre may indicate an artifact caused by the collection methods employed. Genera such as Myrmelachista and Tapinoma, usually found in vegetation, may not have been collected due to the lack of specific methods for this stratum in our inventory. Therefore, although we have added many new records for the state, many more may still be made as collections are carried out targeting other strata.

The new records of the species Linepithema piliferum, Pheidole cuevasi, Pheidole demeter, and Pheidole gilva in Brazil are expected, since they all have records in Peru, country that borders the PNSD. Although the records of species Apterostigma callipygium, and Pheidole sagax are not unexpected, the new findings presented in this study represent a significant extension of their distribution range, which was previously more closely documented in Ecuador and Colombia.

The area of PNSD was strongly influenced by the Andes during its geological and floristic formation (SEMA 2010). Its location in a transitional zone between the Andes and the Amazon likely contributes to the high biodiversity observed in the extreme west of Acre, as suggested by Ruaro & Laurance (2021). Additionally, the relatively low rate of accumulated deforestation (28.43 km2 between 2008 and 2023) and low human density in the park contribute to the protection of PNSD’s fauna from direct anthropogenic effects (Bardales et al. 2023, TerraBrasilis Portal – INPE 2024).

Finally, the results found in the present study emphasize the park’s strategic significance for the conservation. In fact, the number of ant species newly recorded for the state of Acre (66), for Brazil (6), and the number of species potentially identified as new for science (22) is the most significant considering all recent surveys conducted in under-sampled regions of the western Amazon (Feitosa et al. 2022). These numbers are a strong indication that the PNSD is among the areas with the highest diversity of ants on the planet, even when compared to other conservation units with much greater sampling efforts. This finding underscores the importance of maintaining the PNSD as a National Park, ensuring the highest level of legal protection for the area.

Supplementary Material

The following online material is available for this article:

Table S1 – Supporting information: Frontier Ants Unveiled: Exploring the Remarkable Diversity of the Brazilian far west.

Acknowledgments

We thank Alexandre Casadei-Ferreira and Thiago Silva for their assistance in collecting the ants. We also express our gratitude to Eder França, Frederico Marcineiro, Paloma Andrade, Jaqueline Paes, Lívia Prado, Otávio Silva, and Alexandre Casadei-Ferreira for their support with species identifications. Ant collection was conducted under research permit SisBio 38818-6, issued by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). We acknowledge the financial support provided by the National Council of Research and Scientific Development – CNPq (grants 301495/2019–0 and 140811/2019-2). This paper was also partially funded by the Partnerships for Enhanced Engagement in Research (PEER) Science Program (NAS/USAID – award number AID-OAAA-11-00012 – project 3-188).

Data Availability

Supporting data are available at: 10.5281/zenodo.12709586

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Publication Dates

  • Publication in this collection
    02 Dec 2024
  • Date of issue
    2024

History

  • Received
    13 July 2024
  • Accepted
    28 Oct 2024
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