Cyatta abscondita: Taxonomy, Evolution, and Natural
History of a New Fungus-Farming Ant Genus from Brazil
Jeffrey Sosa-Calvo1,2*, Ted R. Schultz2*, Carlos R. F. Brandão3, Christiana Klingenberg4, Rodrigo M.
Feitosa5, Christian Rabeling6, Maurício Bacci Jr.7, Cauê T. Lopes8, Heraldo L. Vasconcelos8
1 Maryland Center for Systematic Entomology, Department of Entomology, University of Maryland, College Park, Maryland, United States of America,
2 Department of Entomology, National Museum of Natural History, SmithsonianInstitution, Washington, District of Columbia, United States of America, 3 Museu
de Zoologia, Universidade de São Paulo, São Paulo, São Paulo, Brazil, 4 Abteilung Entomologie, Staatliches Museum für Naturkunde, Karlsruhe, Karlsruhe,
Germany, 5 Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil, 6 Museum of Comparative Zoology, Harvard University,
Cambridge, Massachusetts, United States of America, United States of America, 7 Centro de Estudos de Insetos Sociais, Universidade Estadual Paulista, Rio
Claro, São Paulo, Brazil, 8 Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil
Abstract
Cyatta abscondita, a new genus and species of fungus-farming ant from Brazil, is described based on morphological
study of more than 20 workers, two dealate gynes, one male, and two larvae. Ecological field data are summarized,
including natural history, nest architecture, and foraging behavior. Phylogenetic analyses of DNA sequence data from
four nuclear genes indicate that Cyatta abscondita is the distant sister taxon of the genus Kalathomyrmex, and that
together they comprise the sister group of the remaining neoattine ants, an informal clade that includes the
conspicuous and well-known leaf-cutter ants. Morphologically, Cyatta abscondita shares very few obvious character
states with Kalathomyrmex. It does, however, possess a number of striking morphological features unique within the
fungus-farming tribe Attini. It also shares morphological character states with taxa that span the ancestral node of the
Attini. The morphology, behavior, and other biological characters of Cyatta abscondita are potentially informative
about plesiomorphic character states within the fungus-farming ants and about the early evolution of ant agriculture.
Citation: Sosa-Calvo J, Schultz TR, Brandão CRF, Klingenberg C, Feitosa RM, et al. (2013) Cyatta abscondita: Taxonomy, Evolution, and Natural History
of a New Fungus-Farming Ant Genus from Brazil. PLoS ONE 8(11): e80498. doi:10.1371/journal.pone.0080498
Editor: Ben J Mans, Onderstepoort Veterinary Institute, South Africa
Received August 13, 2013; Accepted October 3, 2013; Published November 15, 2013
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by
anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: The authors gratefully acknowledge their funding sources: TRS was supported by United States National Science Foundation grant DEB
0949689 and by the Smithsonian Institution Scholarly Studies Program. TRS and JSC were supported by the Smithsonian National Museum of Natural
History (NMNH) Small Grants Program. CR was supported by the Harvard Society of Fellows. MB was supported by the Fundação de Amparo à Pesquisa
do Estado de São Paulo (FAPESP) (2006/00185–7) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)(476250/2008–0 and
310826/2006–3). JSC was supported by a Max and Vera Britton Environmental Science Award (Cosmos Club Foundation) and a Peter Buck Pre-doctoral
Fellowship (NMNH–SI). RMF was supported by FAPESP (2011/24160–1). CRFB was supported by FAPESP and CNPq. The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: sossajef@si.edu (JSC); schultzt@si.edu (TRS)
Introduction
was described as recently as 2002 [4–8] (currently considered
a suborder of Notoptera [9]).
Despite their status as a relatively well-studied group, ants
(Formicidae) are no exception to this trend of increasing
species discovery [10]. Over 12,700 ant species in 308 genera
have so far been described [11,12], yet most ant systematists
estimate that there are twice as many extant species [13,14],
which would make ants the most speciose family of social
insects [12]. In recent years, more than 19 new extant and ca.
17 extinct ant genera and one subfamily (Martialinae) have
been described [15–36].
Fungus-farming "attine" ants are exclusively New World in
distribution, ranging from the United States in the North to
Argentina in the South [37–39] with six genera (Acromyrmex,
Atta, Cyphomyrmex, Mycetophylax, Mycocepurus, and
New insect species are being discovered at a rate that is at
least twice the historical average [1–3]. As we might expect,
many newly discovered species are cryptic species (i.e.,
multiple species previously thought to comprise a single
species) and/or are easily referable to well-known genera or
species groups. A significant number of newly discovered
species, however, are phylogenetically important, i.e., they are
the sole representatives of previously unknown, anciently
diverged lineages and, as such, sources of new information
about early insect evolution. New supraspecific taxa (e.g., new
genera, families, etc.) are commonly erected for such species.
For example, a new order of insects, the Mantophasmatodea,
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Cyatta: A New Genus of Fungus-Farming Ants
Trachymyrmex) also present in the Caribbean [30,39,40]. To
date, 256 valid species have been described in 15 extant
genera and in one ichnogenus (Attaichnus Laza) [11,30].
Because attine ants participate in complex associations with
their cultivated fungi and other microbial symbionts, they have
become model systems for the study of symbiosis and
coevolution [41–61]. Attine ants have additionally become
model systems for comparative evolutionary studies of mating
frequency/polyandry, gyne number, parthenogenesis, social
parasitism, caste polyethism and polymorphism, nesting
behavior, foraging behavior, and diverse microbial symbioses
[47,48,57,62–70]. Leaf-cutter ants in particular are the subjects
of a century of applied research due to their status as serious
pests of agriculture in Central and South America [71–85].
Here we describe the sole representative species of a new
genus, Cyatta abscondita gen n. et sp n., in the fungus-farming
ant tribe Attini (Formicidae: Myrmicinae) and document its
presence in the Brazilian Cerrado, a global biodiversity hotspot
[86]; in the Caatinga, a xeric shrub-land and thorn forest in
northeastern Brazil; and in Atlantic semi-deciduous forest,
considered a transitional zone between humid Atlantic forests
and the drier biomes of the Caatinga and Cerrado [87]. We
describe the morphology, behavior, fungal associations, nest
architecture, and other biological characters of C. abscondita
that are potentially informative about plesiomorphic character
states within the tribe Attini and within the informal clade
Neoattini and, consequently, about the early evolution of ant
farming behavior.
Composite images were assembled using Auto-Montage Pro®
(Version 5.03.0061 BETA) software (Synoptics Ltd.). Images of
the male were generated at the MCZ using a Leica DFC 420
digital camera mounted on a Leica MZ16 dissecting scope.
Composite images were assembled using Leica Application
Suite (Version 4.0) and Helicon Focus (Version 5.3) software
packages. The only two larvae collected were dehydrated
sequentially through a series of ethanol concentrations to
100% absolute and then critical-point dried in a Balzers CPD–
030 using liquid CO2 at the Scanning Electron Microscopy
(SEM) Lab in the SI–NMNH. Once the ethanol was replaced
with CO2 the samples were slowly heated to the critical point,
slowly depressurized back to atmospheric pressure, dried, and
mounted on aluminum stubs. The two prepared larvae and an
adult worker Paratype were sputter-coated with 60:40 wt%
Gold:Palladium alloy on a Cressington Scientific 108 auto/SE
sputter coater to a thickness of 20–25 nm. Scanning Electron
Micrographs (SEMs) of these specimens were generated using
a Philips XL–30 ESEM with Lanthanum Hexaboride (LaB6)
source and with a backscatter detector. All images were
cropped and edited using Photoshop CS5® (Version 12.0)
(Adobe Inc.).
The
measurements,
indices,
abbreviations,
and
morphological terminology utilized throughout follow Gauld &
Bolton [88], Klingenberg & Brandão [30], Rabeling et al. [89],,
Serna & Mackay [90], and Sosa-Calvo & Schultz [91] and
literature cited therein, with modifications where noted.
Characters and terminology used in the description of the
larvae are based on Schultz & Meier [92]. The following
abbreviations are used in the description: w= worker, dg=
dealate gyne, m= male.
Latitude and longitude coordinates were converted to
decimal degree when needed by using the Earth Point Web
Site (http://www.earthpoint.us/Convert.aspx). In cases where
coordinates were not documented in the specimen label, the
coordinates were estimated using Google Earth v7.0 (http://
www.google.com/earth/index.html) and are presented within
brackets. The distribution map of Cyatta abscondita was
generated using the software ArcGIS v10.1 (Esri, Redlands,
CA).
Materials and Methods
Material examined
The specimens examined have been deposited in the
following institutions:
BLME Coleção Entomológica, Bacci Laboratory of Molecular
Evolution, São Paulo State University (UNESP), Rio Claro,
Brazil.
CRC C. Rabeling Collection, Cambridge, MA, U.S.A.
DZUP Coleção Entomológica “Pe. Jesus Santiago Moure”,
Departamento de Zoologia, Universidade Federal do Paraná,
Curitiba, PR, Brazil.
MCZ Museum of Comparative Zoology, Harvard University,
Cambridge, MA, U.S.A.
MZSP Museu de Zoologia, Universidade de São Paulo, São
Paulo, Brazil.
MBC–UFU Museu de Biodiversidade do Cerrado,
Universidade Federal de Uberlândia, Uberlândia, Minas
Gerais, Brazil.
USNM United States National Museum of Natural History,
Washington, DC, U.S.A.
Field observations and nest excavations
Field work was conducted at Fazenda Água Limpa from 20–
27 February 2009 (JSC, TRS), 12–18 April 2010 (JSC, TRS,
CTL), and 14–22 September 2011 (JSC, TRS, CTL); and at the
Broa preserve from 21–28 July 2011 (CR, MB). Fazenda Água
Limpa (FAL) is a 4490 ha experimental farm and conservation
area of the Universidade de Brasília located at S15.94938°
W47.93567°, ~30 km from Brasília, DF, Brazil, at an altitude of
1048–1160 m. The Broa preserve, one of the southernmost
Cerrado preserves of São Paulo state, is located at
S22.18517° W47.87754°, 9.5 km northwest of Itirapina in São
Paulo state, Brazil, at an altitude of 530 m.
At FAL, nest entrances were located by following foragers
carrying bait (Cream of Rice cereal liberally distributed on the
ground) as they returned to the nest. Nests were excavated by
first digging a trench about 1 meter wide and 1.5 meters deep
and located about 1 meter from the nest entrance, and then by
Morphological measurements and specimen
preparation
All measurements were taken to the nearest 0.001 mm and,
unless otherwise noted, are in millimeters. Images of worker
and gyne were generated at the USNM Ant Lab using a JVC
KY–F75U digital camera mounted on a Leica Z16 APO
steromicroscope attached to a Dell Optiplex GX620 computer.
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Cyatta: A New Genus of Fungus-Farming Ants
Table 1. Colony demographies and nest measurements of six excavated Cyatta abscondita nests, including depths and
dimensions of individual chambers, chamber contents, fungus garden morphology, ant demographics, and additional natural
history information.
CHAMBER DIMENSIONS (cm)
Chamber
Nest Locality Collection code Date
number
Depth (cm) Height
Width
Depth
Demography, garde morphology, notes
1
1
70
3
N/A
2 pendant garden filaments
2
70
1.5
2.5
N/A
empty; 3 polydesmid millipedes
3
~75
2.5
5
5
24 pendant garden filaments
2
3
4
5
6
FAL
FAL
FAL
FAL
Broa
Broa
JSC100412-01
JSC100416-01
April 12-18, 2010
April 17-18, 2010
1.2
4
80
2.5
3.5
N/A
pendant garden; 8 workers (1 callow)
1
40
0.5
1
N/A
small pendant garden; no ants
2
46
1.5
2.5
N/A
small pendant garden; 2 workers
3
50
0.5
1
N/A
empty
4
55
2
3
N/A
small pendant garden; 2 workers
5
56
2.6
3
N/A
pendant garden; 2 workers
6
61
2.5
5.5
N/A
empty
7
71
2.5
3
N/A
pendant garden; some workers; dealate gyne
September 19, 2011 1
29
1.5
5.5
1.3
empty
2
35
2
3
1.2
pendant garden; 1 workers
3
44
1.5
2
0.5
September 20, 2011 1
38
2
3
1
2
42
3
2
2
2 workers
3
43.5
2
2.5
3
2 workers
4
46
2
3
1.5
15-20 pendant garden filaments
5
50
1.5
1.5
1.5
small pendant garden; 2 workers
6
59.5
1.5
3.5
1.2
large pendant garden; 7 workers
7
82
1.8
2.5
3
large pendant garden; 4 workers
8
104
1.9
4
3.5
1
52
1.5
3
N/A
CR110721-04
2
80
1.5
5
N/A
CR110721-08
3
130
1
2.5
N/A
CR110721-07
4
160
?
?
?
1
102
?
?
?
2
195
1
3
N/A
JSC110919-02
JSC110920-01
CR110721-05
CR110726-09
July 21, 2011
July 26-28, 2011
CR110728-01
small pendant garden; a couple of workers;
dealate gyne
small pendant garden
large pendant garden; several workers; larvae;
dealate gyne
fungus garden; 13 workers
~50 pendant garden filaments; 10 workers; 1
male
fungus garden; 3 workers
fungus garden; no ants; chamber collapsed
during excavation
fungus garden; 3 workers; chamber collapsed
during excavation
fungus garden; 4 workers
For each nest, chambers are arranged according to depth, descending from the shallowest to deepest chambers. Chamber height refers to the chamber's vertical axis,
chamber width to the horizontal axis parallel to the plane of excavation, and chamber depth to the horizontal axis perpendicular to the plane of excavation. FAL: fazenda
Água Limpa, Brasília; Broa: Broa preserve, Itirapina; see text for more details.
doi: 10.1371/journal.pone.0080498.t001
carefully shaving away soil in the direction of the nest entrance
until either tunnels or nest chambers were encountered; see
93,94 for a detailed description of the methodology. During the
course of the excavation, the trench was deepened as
necessary and the dimensions, depths, and relative positions
of tunnels and chambers were measured, photographed, and
sketched. Fungus gardens were transferred from subterranean
chambers to plastic containers with flame-sterilized spoons,
knives, and/or forceps. Colonies were maintained in live culture
in plastic containers, the bottoms of which were lined with
plaster saturated with water. At Broa, nest contents were
preserved in 95% ethanol after a few days, once the ants had
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reconstituted and restabilized their fungus gardens and
removed all soil particles. Two FAL nests (JSC110920-01 and
JSC110919-02) were maintained in live culture for up to four
months (nest 4, see Table 1).
Prior to 2009, only four isolated specimens had turned up in
mass-collected ant samples. These include, from a leaf-litter
sample, one specimen from riparian forest or Cerradão at
Fazenda Olho D’água [611m; S18.90628° W45.53527°],
Paineiras, Minas Gerais (MG), collected in 1999 and, from
pitfall trap samples, one specimen from Caatinga at Reserva
Particular do Patrimônio Natural (RPPN) Serra das Almas
[330m; S05.16479° W40.67978°], Crateús, Ceará (CE), in
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Cyatta: A New Genus of Fungus-Farming Ants
Divergence time estimation
2003 and two specimens from Cerrado sensu stricto from the
Reserva Ecológica do Instituto Brasileiro de Geografia e
Estatística (IBGE) (1100m; S15.85000° W48.05000°), DF,
Brasília, in 2008. More recently, in 2011, four additional stray
specimens were taken in pitfall traps in Cerrado sensu stricto at
Reserva Particular de Patrimônio Natural (RPPN) do Acangau
(671m; S17.1790833° W 47.0583056°), Paracatu, Minas
Gerais (MG), and in fragments of semideciduous forest at
Fazenda Águas Claras (494m; S21.4023° W48.6873°),
Pindorama, São Paulo (SP), and at Estação Experimental
(414m; S21.5222° W49.3013°), Sales, (SP).
The time of divergence of the new genus Cyatta was
estimated using the Bayesian uncorrelated lognormal approach
as implemented in the program BEAST v1.7.5 [102] using a
normal prior distribution for the root age (as described in
Schultz & Brady [95]). Beast XML files were generated using
the complementary program BEAUti v1.7.4 (as implemented in
the BEAST package). The results combine two runs of 100
million generations each. Burn-in, convergence, and mixing
were assessed by examining time series plots and ESS values
in Tracer 1.5.0 [101]. Based on this information, burn-in was
set at 20 million generations for each run.
Permits
Nomenclatural acts
Research and export permits for field work by JSC, TRS,
CTL, and HLV were issued by the Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq; Portarias
No. 267, 359) and the Instituto Brasileiro do Meio Ambiente e
dos Recursos Naturais Renováveis (IBAMA; permit numbers
14789–1, 147892, 14789–3). Dr. Yves P. Quinet and
Francyregis Nunes allowed CRFB and RMF to study the only
known specimen from the Caatinga and supported them during
field work in Crateús. Prof. José Mauro da Silva Diogo,
Director, allowed JSC, TRS, and CTL to work at FAL. The
Fundação Acangau permitted HLV to collect at RPPN do
Acangau.
The electronic edition of this article conforms to the
requirements of the amended International Code of Zoological
Nomenclature ([103]), and hence the new names contained
herein are available under that Code from the electronic edition
of this article. This published work and the nomenclatural acts it
contains have been registered in ZooBank, the online
registration system for the ICZN. The ZooBank LSIDs (Life
Science Identifiers) can be resolved and the associated
information viewed through any standard web browser by
appending the LSID to the prefix "http://zoobank.org/". The
LSID for this publication is: urn:lsid:zoobank.org:pub:
1CF00B3D-CE25-456A-8D12-6DDA628BC110. The electronic
edition of this work was published in a journal with an ISSN,
and has been archived and is available from the following
digital repositories: LOCKSS [http://www.lockss.org] and
PubMed Central [http://www.ncbi.nlm.nih.gov/pmc].
Molecular phylogenetics
DNA extraction, amplification, and sequencing were carried
out at the Laboratories of Analytical Biology (LAB) at the
National Museum of Natural History, Smithsonian Institution,
Washington, DC. Ant genomic DNA was extracted from a
worker collected at FAL, Brasília using the Qiagen DNEasy
Tissue Kit. Four nuclear protein-coding genes, elongation
factor 1-alpha paralog F1 (EF1α F1), elongation factor 1-alpha
paralog F2 (EF1α F2), wingless (wg), and long wavelength
rhodopsin (LW Rh) were amplified and sequenced following
methods outlined in previous studies [95,96]. Sequences are
deposited in GenBank as accession numbers KF569882KF569887.
DNA sequences, consisting of ~2.5 kbp, were added to the
aligned data set of Schultz & Brady [95] and aligned by eye in
MacClade 4.08 [97]. Data were partitioned and modeled as in
Schultz & Brady [95] and analyzed using MrBayes 3.1.2 [98]
with two independent runs of 10 million generations, each
distributed over eight chains (seven heated and one cold;
temperature parameter 0.05). To avoid known problems with
branch-length estimation [99], [100], branch length priors were
shortened as follows: prset applyto = (all) brlenspr =
unconstrained:exponential (100). For each partition, we applied
moderately informative Dirichlet priors to the rate multipliers.
Burn-in and stationarity were assessed by comparing the mean
and variance of log likelihoods, both by eye and by using the
Bayes Factor comparison in Tracer 1.5.0 [101]; by examination
of the MrBayes ".stat" output file; and by examination of the
split frequencies diagnostic. Based on this information, burn-in
was set at 1 million generations.
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Results
Taxonomy
Cyatta
gen.
n.
urn:lsid:zoobank.org:act:
0ED4A047-327E-482C-A6AF-E92136DB5697
Figures 1–4.
Type species.
Cyatta abscondita sp. n., by present
designation.
Worker. Small, monomorphic attine ant, total length (TL)=
2.29–2.56; Weber’s length (WL)= 0.58–0.65. Color pale yellow
to light brown. Body densely reticulate and covered with minute
simple appressed hairs, more abundant on dorsum of head,
waist segments, and gaster than on mesosoma. Palp formula
4,2. Anterior margin of clypeus produced into a convex, almost
triangular, smooth, shining flange, i.e., "clypeal apron," with
long unpaired median seta that originates closer to its posterior
margin. Psammophore absent. Masticatory margin of
mandibles 4-toothed. Antennal scrobes and preocular carinae
absent. Antennae 11-segmented. Frontal lobes reduced, barely
covering antennal insertions and diverging anteriorly. Frontal
area subtriangular, distinct. In full-face view, posterior cephalic
margin inflated laterally and strongly notched medially.
Tubercles on mesosomal dorsum short, attenuate, and blunt.
Metapleura with two spiniform processes between mid and
hind coxae. Propodeum armed with a pair of short triangular
spines. Node of petiole high, well-developed. Gaster lacking
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Cyatta: A New Genus of Fungus-Farming Ants
carinae or tubercles. In lateral view, pygidium rounded, laterally
overlapping and concealing the hypopygium; in ventral view,
pygidium posteromedially emarginate (i.e., V–shaped), the
triangular hypopygium fitting within the emargination of the
pygidium.
Gyne. Preocular carina absent. Mandible 4-toothed, apical
tooth nearly twice as long as preapical tooth. Parapsidal lines
inconspicuous.
Male. Mandibles broadly triangular with apical and subapical
teeth present. Anterior margin of clypeus (clypeal apron)
convex, projecting over mandibles, and with a long median
seta. Discal cell present in forewing.
Etymology. Cyatta is a neologism constructed in part from
the Brazilian Tupi language word Cy, meaning "sister,"
referring to its status, along with the genus Kalathomyrmex, as
the sister clade to the remaining genera of the informal clade
Neoattini, to which the genus Atta, the most conspicuous
member of the Neoattini, belongs.
Calvo & TR Schultz); stray worker; JSC100416-08” [1w,
USNM, USNMENT00521890 (EtOH vial)]. Same data as
previous entry, but “15.iv.2010; (J Sosa-Calvo & TR Schultz);
nest
entrance;
JSC100415-03”
[4w,
USNM,
USNMENT00521907 (EtOH vial)]. BRAZIL: CE: Crateús;
Croatá; RPPN Serra das Almas; [330m; 40.67978° W
05.16479° S]; 20–30.iv.2003; (Y Quinet); pitfall trap; Caatinga,
Carrasco; SP 60 [1w, MZSP]. DF: Brasília; Reserva Ecol.
IBGE; Parcela Bienal Tardia (Projeto Fogo); 1100m; 48.05000°
W 15.85000° S; 30.i.2008; (J Maravalhas); pitfall trap;. Cerrado
sensu stricto; B2/CT [2w, MZSP]. MG: Paineiras; Fazenda
Olho D’Água; [611m; 45.53527° W 18.90628° S]; 22–24.v.
1999; (AA Tavares); Winkler #2; Cerrado [1w, MZSP]. MG:
Paracatu; Reserva Particular de Patrimônio Natural do
Acangau; 671m; 47.0583056° W 17.1790833° S; 12.iv.2011;
(TLM Frizzo); pitfall trap; Cerrado sensu stricto [2w, MBC–
UFU]. SP: Itirapina; 9.5 km northwest of Itirapina; Broa
preserve; 530m; 47.87754° W 22.18517° S; 21.vii.2011; (C
Rabeling & M Bacci Jr); nest series; Cerrado sensu stricto;
under
ground;
CR110721-04
[1w,
MZSP,
USNMENT00758220; 1m, MZSP, USNMENT00758204], [1w,
MZC,
USNMENT00758221],
[2w,
USNM,
USNMENT00758219, USNMENT00758222], [6w, BLME &
CRC, USNMENT00758190–95]. Same data, but CR110721-05
[1w,
MZSP,
USNMENT00758217],
[1w,
MZC,
USNMENT00758218], [1w, USNM, USNMENT00758206],
[10w,
BLME
&
CRC,
USNMENT00758207,
USNMENT00758253–61]. Same data, but CR110721-08 [3w,
BLME & CRC, USNMENT00758196–98]. Same data, but
26.vii.2011,
CR110726-09
[3w,
BLME
&
CRC,
USNMENT00758199–201]. Same data, but 28.vii.2011,
CR110728-01 [3w, BLME & CRC, USNMENT00758262-65],
[1w, USNM, USNMENT00758205]. SP: Pindorama; Fazenda
Águas Claras; 494m; 48.6873° W 21.4023° S; 16.viii.2011; (GA
Castilho); Floresta Estacional Semidecidual; pitfall B1 [1w,
MZSP]. SP: Sales; Estação Experimental; 414m; 49.3013° W
21.5222° S; 17.viii.2011; (GA Castilho); Floresta Estacional
Semidecidual; pitfall I4 [1w, MZSP].
Measurements. TL 2.03–2.60, WL 0.52–0.66, HL 0.48–
0.55, HW 0.46–0.54, SL 0.42–0.51, ML 0.20–0.38, EL 0.10–
0.14, PL 0.13–0.19, PPL 0.21–0.25, GL 0.47–0.59, CI 87–95,
SI 91–104, MI 40–68, FLD 0.16–0.18 (n=13).
Etymology. The specific name "abscondita" refers to the
exceedingly secretive nature of this species, which, after being
recognized from a few rare specimens, proved frustratingly
elusive during multiple attempts to locate it in the field.
Worker. Head. in full-face view subrectangular, slightly
longer than wide (CI 87–95); sides subparallel. Mandible
subtriangular with four well-developed teeth; apical tooth twice
as large as subapical tooth; diastema between subapical tooth
and 3rd tooth shorter or slightly shorter than diastema between
3rd and 4th teeth (Figure 2c); dorsum of mandible reticulate and
with appressed hairs (Figure 2d); masticatory margin of
mandible, including apical tooth, smooth, shining, and darker in
color than rest of head, with long, simple hairs. Clypeal apron
(anteclypeus) convex to almost triangular, smooth, and shining;
unpaired median setae (length 0.07–0.10 mm) originating
slightly before (anterior to) posterior edge of clypeal apron and
Cyatta abscondita, sp. n
urn:lsid:zoobank.org:act:3260572CB7CE-429C-9440-27613BDBE69E
Holotype, worker. labeled: “BRAZIL: DF: Brasília; Faz.
Água Limpa; 1106 m; 47.90133° W 15.9524° S ±5m; 20.ix.
2011; (J. Sosa-Calvo, T.R. Schultz, C.T. Lopes); nest series;
Cerrado sensu stricto; in ground; JSC110920-01” [MZSP,
unique specimen identifier No. USNMENT00758173].
Paratypes.
same data as holotype [3w, MZSP,
USNMENT00758172, 00756921, 00758307], [1dg, 4w, USNM,
USNMENT 00758174, 00758223, 00758316–18] [3w, USNM,
USNMENT00521881 (EtOH vial)]. Same data as holotype, but
“19.ix.2011;
JSC110919-02”
[1dg,
MZSP,
USNMENT00758175], [2w, USNM, USNMENT00758176–77]
[1w, USNM, USNMENT00521910 (EtOH vial)]. Same data as
holotype, but “16.iv.2010; JSC100416-04” [1w, MZC,
USNMENT00758180] [1w, USNM, USNMENT00521908 (EtOH
vial)]. Same data as holotype, but “1099 m; 47.90129° W
15.95242° S ±3m; 23.ii.2009; (J Sosa-Calvo & TR Schultz);
nest series on ground; JSC090223-26” [1w, USNM,
USNMENT00758178]. Same data as previous entry, but “16.iv.
2010; nest series underground; JSC100416-01” [1w, DZUP,
USNMENT00758319] [2w, 1dg (currently misplaced) USNM,
USNMENT00758323–24,
00758325]
[3w,
USNM,
USNMENT00521886 (EtOH vial)]. Same data as holotype, but
“Garden near dorms; 1071 m; 47.93567° W 15.94938° S ±3m;
12.iv.2010; (J Sosa-Calvo, TR Schultz, CT Lopes); nest series;
back yard; under ground; JSC100412-01” [1w, DZUP,
USNMENT00758224], [1w, MZSP, USNMENT00758179], [3w,
USNM,
USNMENT00758320–22]
[3w,
USNM,
USNMENT00521917 (EtOH vial)].
Worker measurements. Holotype (Paratypes, n=9). TL
2.40 (2.29–2.56), WL 0.62 (0.58–0.65), HL 0.53 (0.50–0.55),
HW 0.48 (0.48–0.51), SL 0.48 (0.43–0.50) ML 0.34 (0.32–
0.36), EL 0.13 (0.12–0.13), PL 0.17 (0.14–0.19), PPL 0.22
(0.20–0.24), GL 0.52 (0.49–0.64), CI 90 (90–95), SI 101 (90–
100), MI 64 (63–68), FLD 0.17 (0.17–0.18).
Additional material examined. Same data as holotype, but
“1099 m; 47.90129° W 15.95242° S ±3m; 16.iv.2010; (J Sosa-
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 1. Holotype worker (USNMENT00758173) (A, C, E) and Paratype gyne (USNMENT00758174) (B, D, F) of Cyatta
abscondita. (A, B) Full-face view. (C, D) Lateral view. (E, F) Dorsal view.
doi: 10.1371/journal.pone.0080498.g001
almost or as long as antennal pedicel, not reaching apex of
mandible (Figures 2c,d); clypeus with pair of lateral transverse
carinae, each extending from below frontal lobe to mandibular
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insertion. Medially these carinae developed into lamellae
perpendicular to clypeal face, thus forming a wall that divides
the clypeus laterally into anterior and posterior areas, very
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Cyatta: A New Genus of Fungus-Farming Ants
margins slightly diverging posteriorly; posterior margin with
deep median impression, forming two distinct small lobes; in
lateral view, anterior portion of postpetiole convex, postpetiole
relatively compressed dorsoventrally; ventral projections
absent (Figures 1c,e). In profile, gaster elliptical and dorsally
finely reticulo-striate; in dorsal view, apical margin of pygidium
(gastral segment IV, i.e., abdominal segment A7) medially
emarginate, bilobed; gastral sternite IV (hypopygium, i.e., A7)
covered with simple decumbent hairs; in lateral view, pygidium
rounded, laterally overlapping and concealing the hypopygium;
pygidium weakly reticulate and shiny; in ventral view, pygidium
posteromedially emarginate (i.e., V–shaped), the triangular
hypopygium fitting within the emargination of the pygidium
(Figures 2e,f). Sting apparatus present, protruding through
emargination on pigydium.
Color pale yellow to light brown; antennae, mandibles, and
legs lighter than rest of body. Body integument areolate, with
short appressed simple hairs, appearing almost hairless.
Gyne. As in worker description, but with caste-specific
morphological differences as follows. All gynes studied are
dealate. Head: Eyes large, with 10–11 ommatidia in maximum
length and 9 ommatidia in maximum width, ~65 ommatidia
total; median ocellus rounded, located in a median sulcus
extending almost from the occipital carina in the back of the
head to the middle of the frons; integument surrounding ocelli
darker in color than elsewhere. Clypeus with unpaired median
seta arising on short transverse wrinkle-like ridge that crosses
clypeal apron; two to four short simple appressed hairs on
clypeal apron on each side of median clypeal seta. In full-face
view, cephalic border with median (vertexal) notch, not as deep
as in worker. Mandibles dorsally coarsely rugose.
Mesosoma.
Pronotal dorsum conspicuously areolate,
lacking anterior pronotal tubercles; lateral pronotal tubercles
present, blunt and small; humeral pronotal tubercles vestigial.
Mesoscutum, in dorsal view, rounded to slightly ovate and
overall reticulo-rugose; dorsum of mesoscutum, in profile,
almost flat; mesoscutal sulcus, in dorsal view, short, not
extending more than 1/4 length of mesoscutum; notauli absent;
parapsidal lines short, inconspicuous, and extending nearly to
lateral margin of mesoscutum; transscutal suture conspicuous.
Scuto-scutellar sulcus deep and with ~7 transverse carina;
margin of axilla rounded, dorsally reticulo-rugose. Scutellum
posteriorly weakly bidentate, dorsally rugose and with a
shallow median longitudinal groove. Anapleural sulcus deep,
with transverse carinae, dividing mesopleuron into
anepisternum and katepisternum. Metanotal groove extended
into a complete metanotal-propodeal suture (sensu Serna &
Mackay [90]). In profile, metanepisternun (sensu Serna &
Mackay [90] present, small. In profile, metanotal groove
conspicuous, continuous with mesometapleural suture. Ventral
metapleural processes present as a pair of spiniform tubercles
between the mid and hind coxae, similar to, but longer than,
those present in worker. Propodeum with pair of short, rightangled denticles; dorsum, lateral margin, and declivity of
propodeum reticulate. Metasoma: petiole as in worker. Dorsum
of postpetiole reticulo-rugose. Dorsum of gastral tergite IV (A7)
rugulose; pilosity as in worker; gastral tergite and sternite IV
(pygidium and hypopygium; A7) as in worker.
likely homologous with clypeal morphology of closest relative,
Kalathomyrmex emeryi (Figure 2c); medially clypeus is not so
divided, face extending posterad between frontal lobes. Frontal
lobes reduced, convex, barely covering antennal insertions
(Figures 1a, 2c). Frontal carina fading out posteriorly at
midlength of compound eye (Figures 1a, 2c). Well marked
triangular area with concave anterior margin between frontal
lobes reticulate, bordered anteriorly by rounded finger of
clypeus, which extends broadly posterad between frontal lobes.
Compound eye set slightly before middle of head, with 7–9
ommatidia at maximum length and 6 ommatidia at maximum
width (33–47 ommatidia in total). Antennal scape covered with
minute, simple, appressed hairs; antennal scape wider at
seven-tenths of its length, and slightly surpassing
posterolateral corners of head when laid back over head
capsule; first funicular segment (pedicel) slightly longer than or
as long as second and third funicular segments combined. In
full-face view, cephalic margin deeply notched medially (i.e., at
vertex) and rounded laterally (Figure 1a), shallow vertexal
sulcus extending medially towards frontal lobes, fading at eye
level; in lateral view, ventral face of head slightly convex.
Hypostomal teeth absent. Palp formula 4,2 (Figures 2a,b).
Mesosoma. Profile of promesonotal dorsum in lateral view
distinctly tuberculate, tubercles attenuate and blunt (Figures
1c,e, 2a). In dorsal view, promesonotum with raised shield-like
area, broad anteriorly and narrowing posteriorly, distinctly
separated from lower, lateral promesonotum; raised area
formed anteriorly by triangular lateral pronotal tubercles and
two median low and approximate pronotal tubercles and
posteriorly by eroded remnants of promesonotal tubercles;
lower, lateral area of promesonotum in dorsal view
subtriangular, broader and anterolaterally angled anteriorly; in
lateral view, inferior corner of pronotum rounded, lacking
spines or angles. Anepisternum indistinctly separated from
katepisternum. Metanotal groove relatively broad and strongly
impressed, in lateral view extending to antero-ventral margin of
metapleuron. Metapleura ventrally with two spiniform
processes between mid and hind coxae, best seen by
removing hind legs. Basal (dorsal) face of propodeum in lateral
view a low, rounded, protuberance posterior to metanotal
groove; in dorsal view, basal face very small, raised above
remainder of propodeum, and narrowing anteriorly; declivous
face of propodeum behind protuberance concave; propodeal
spines triangular (Figure 1c), obliquely directed upwards and
strongly diverging in dorsal view; declivity of propodeum much
longer than base (dorsum); propodeal spiracle opening in an
angle of 45° in relation to main body axis; in lateral view,
propodeal lobes rounded without posterior projections.
Peduncle of petiole vestigial; in lateral view, petiolar node
well developed, subquadrate, with anterior face almost straight
and vertical; dorsum of petiolar node short and almost flat,
meeting vertical posterior face in slightly rounded angle; ventral
face of petiole slightly concave or straight medially, lacking
petiolar process (Figures 1c,e); in fronto-dorsal view, node of
petiole shallowly V shaped, dividing node into a pair of rounded
tubercles. Postpetiole robust, almost twice as long as petiole
and slightly less than 0.5x gaster length; in dorsal view,
postpetiole subtriangular, anterior margin rounded, lateral
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 2. Paratype worker (USNMENT00758223) of Cyatta abscondita. (A) Habitus, lateral view. (B) Head, lateral view,
indicating palp formula. (C) Head, full-face view. (D) Clypeal apron indicating origin of median unpaired seta. (E) Metasoma,
posterior view. Pygidium (p) ‘V’-shaped, hypopygium (hyp) triangular. (F) Metasoma, ventral view, showing the median emargination
of the pygidum and the triangular shape of the hypopygium.
doi: 10.1371/journal.pone.0080498.g002
Measurements. TL 3.27–3.32, WL 0.86–0.87, HL 0.65–
0.66, HW 0.60–0.63, SL 0.56, ML 0.41–0.42, EL 0.16–0.17, PL
0.25–0.28, PPL 0.29–0.30, GL 0.79–0.81, CI 91–96, SI 89–93,
MI 62–65, FLD 0.20–0.21 (n=2).
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Male. A medium-sized male with head large relative to size
of the mesosoma. Mandibles broadly triangular, apical and
subapical teeth present large; remaining tooth minute,
indistinct; texture coarsely granulate. Palp formula 4,2. Clypeus
broadly trapezoidal in frontal view; anterior margin convex, with
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Cyatta: A New Genus of Fungus-Farming Ants
known to be present only in the larvae of Mycocepurus goeldii
and M. smithii [92], where their presence may be
plesiomorphic, and in Sericomyrmex and some Acromyrmex
species, where their presence is likely secondarily derived.
Predominant hair type bifurcate with "anchor tips" (Figures
4a,d). Two rows of dorsomedian, very long anchor-tipped hairs
present (Figure 4e). Labrum monolobate, narrow, bulging.
Anterior setae present as papillae. Mandibles typically attine:
short, fleshy, subconical. A distinct, undivided apical
mandibular tooth and no subapical teeth; spinules evenly
distributed on all mandibular surfaces. Mandibular gnathobases
absent. Basal portions of maxillae fused with head capsule.
Maxillary palp widely removed laterad from galea, a
synapomorphy for the Neoattini. Galea reduced, present as two
sensilla surmounting a low protuberance, as in all Attini except
for some Myrmicocrypta species. Maxillary palp digitiform,
maxillary accessory palpal sensillum absent. A single seta
present laterad of maxillary palp, a character shared with
Mycocepurus species. As in most attines, labium feebly
protruding, lateral sericteral protuberances absent, labial palps
digitiform. Labial spinules present on anterior surface slightly
dorsal to the sericteries. Hypopharyngeal spinules multidentate
and apparently densely distributed. On the head, genal lobes
absent, a state in the Attini shared with Myrmicocrypta,
Apterostigma, Mycocepurus, and Mycetarotes species. Supraantennal setae present and abundant, a condition common in
the subfamily but otherwise present in the lower Attini only in
M. goeldii. Subantennal (genal) setal arrangement
plesiomorphic for the tribe, consisting of around 12 setae on
each gena. Supraclypeal setae present and setiform. Two
clypeal setae present. Spinules absent on the head dorsad of
the labrum, the state common to most attines. Due to the poor
condition of specimens, most ventral thoracic/abdominal
characters could not be studied, including the presence/
absence of: leg vestiges, prothoracic food anchor,
ventromedian protuberances on various segments, papilliform
spinules, and hairs.
Two setal sockets occur ventral of the anal opening on
abdominal segment IX (Figure 4f). No other setae are
associated with the anal opening. Ventral anal lip absent.
Comments. The new genus Cyatta shares with other
genera belonging to the tribe Attini: (i) the presence of a thick
unpaired median seta arising from the clypeal apron
(considered a synapomorphy for the tribe by Brandão &
Mayhé-Nunes [105]; but, along with the clypeal apron,
presumed secondarily lost in Kalathomyrmex [30]); (ii) 11
antennal segments in the worker and gyne, 13 in the male (the
latter secondarily reduced in some Cyphomyrmex,
Mycetagroicus, Sericomyrmex, Trachymyrmex, and social
parasites); (iii) palpal formula 4,2 (plesiomorphic for the Attini,
secondarily reduced in Apterostigma and some social
parasites). Larvae of Cyatta share with the larvae of other
attine genera the: (iv) thoracic-abdominal articulation
apparently absent; (v) thoracic intersegmental constrictions
superficial; (vi) deep lateral depressions associated with
abdominal spiracles absent; (vii) short, narrow labrum; and (viii)
fleshy, subconical mandibles. Behaviorally, Cyatta shares with
other Attini the cultivation of fungi for food.
a long median seta (0.11 mm) originating at the anterior margin
and projecting over the mandibles; in lateral view anterior
margin of clypeus forming a lamella projecting over the
mandibles. Frontal lobes triangular, only partly covering the
condylar bulbs of the scape in full face view. Antennae with 13
segments; scape surpassing the posterior border of the head
by 1/3 of its length. Antennal funicular segment II (0.08 mm)
almost as long as funicular segment I (pedicel; 0.11 mm)
(Figures 3a,b). Eyes conspicuously large, at maximum
diameter approximately half as long as the entire head,
counting ~15 ommatidia in maximum width and ~23 ommatidia
in maximum length. Ocelli large, elevated above the remainder
of the head. Surface of head coarsely granulate, finely rugulose
around the ocelli. Tergum of promesonotum not distinctly
enlarged, giving the mesosoma a rather slender appearance in
lateral view. In dorsal view, lateral pronotal teeth pyramidal,
twice as wide at the base than high, with sharp tips. Propodeal
spines reduced to broad teeth with rounded tips. Anterior
peduncle of the petiole about the same length as the petiolar
node. Postpetiole wider than long; trapezoidal in dorsal view;
posterior margin slightly concave. In lateral view, postpetiole
with a broadly rounded ventral lobe. Reticulate sculpture on
gaster finer in appearance than on the remainder of body,
which tends to be areolate; gastric tergites moderately lustrous;
rest of body with a weak silky shine. Body surface sparsely
covered with short appressed setae, only ventral side of
postpetiole with 10 erect setae. Body dark, blackish brown;
legs and antennae slight lighter in color, yellowish to dark
brown. Forewings with closed basal (BC), costal (CC),
submarginal (SMC1), marginal (MC), and subbasal (SBC)
cells; submarginal cell 2 and discal cell 2 open (Figure 3d).
Hindwings with closed basal cell and open marginal subbasal
and discal cells (Figure 3d). Left forewing with closed discal
(DC1) cell, whereas the right forewing lacking this cell. The
presence of a closed discal cell in the forewing is, so far as is
known to us, unique in the Attini; this character is absent in all
other attine genera, including the closest relative of C.
abscondita, Kalathomyrmex emeryi. A closed discal cell is
plesiomorphically present in many ant species, including those
in genera closely related to the Attini such as the
Blepharidattini, Cephalotini, Dacetonini, and Pheidolini.
Measurements. EL 0.25, EW 0.27, FL 0.81, FLD 0.21, GL
0.87, HL 0.58, HW 0.73, IOD 0.42, ML 0.21, MI 37, PL 0.27,
PPL 0.25, PPW 0.38, PrW 0.54, PW 0.21, SL 0.54, TL 3.21,
WL 1.04, CI 126, SI 127 (n=1).
Larva. Description based on SEM study of two specimens,
late- (probably fourth) instar larvae of uncertain (but probably
worker) caste. Due to collapsed condition of specimens,
habitus profile could not be characterized with certainty, but is
consistent with the "attoid" profile category of Wheeler &
Wheeler [104], i.e., with a moderately curved, ventrally
shortened profile. Thoracic-abdominal articulation apparently
absent, thoracic intersegmental constrictions superficial, deep
lateral depressions associated with abdominal spiracles
absent, all states shared with other Attini. Remarkably, body
hairs present dorsally and laterally, a condition otherwise
common in the Myrmicinae but rare in the Attini, in which larvae
usually lack dorsal and lateral hairs. In the Attini, such hairs are
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 3. Male of Cyatta abscondita (USNMENT00758204). (A) Full-face view. (B) Lateral view. (C) Dorsal view. (D) Wings:
forewing (top), hindwing (bottom). Cells: basal (BC), costal (CC), submarginal (SMC1), marginal (MC), subbasal (SBC), and discal
(DC1).
doi: 10.1371/journal.pone.0080498.g003
preapical teeth are the largest and have a multidentate (sawlike) margin.
Cyatta differs from its sister genus Kalathomyrmex, however,
by (i) having, on the forewing of the male (forewing of gyne
unknown), a closed marginal cell (Figure 3d) (open in the
forewings of both the male and gyne of Kalathomyrmex
[Klingenberg and Brandão ([30]), therein as radial cell]); (ii) the
mesoscutum of the male with strongly impressed notauli
(absent in the male of Kalathomyrmex); (iii) the pronotum of the
male with lateral pronotal tubercles present, pyramidal (the
pronotum in the male of Kalathomyrmex lacks any tubercles);
and (iv) the psammophore absent in the worker, the gyne, and
the male.
In addition to the previously mentioned absence of an inferior
pronotal tubercle in adult workers, shared with Kalathomyrmex,
Cyatta differs from all or most other Neoattini in a number of
larval character states shared with the Paleoattini, suggesting
that they may be retained symplesiomorphies, including: (i)
The genus Cyatta shares with other members of the
neoattine clade: (i) the antennal scape of the male long, longer
than the sum of the length of antennal funicular segments I–III;
(ii) the first funicular segment (pedicel) of the antenna of the
male longer than second funicular segment; (iii) the petiole in
workers somewhat sessile; (iv) the lack of hypostomal teeth in
workers and gynes; and (v) the maxillary palp of the larva
widely removed laterad from the galea.
Cyatta shares with its sister genus, Kalathomyrmex, (i) the
lack of a tubercle or spine on the inferior lateral margin of the
pronotum, a symplesiomorphy shared with the paleoattine
clade; (ii) the clypeus with a pair of lateral transverse carinae,
each extending from the frontal lobe to the mandibular insertion
and each medially developed into a lamella perpendicular to
the clypeal face, thus forming a wall that divides the clypeus
laterally into anterior and posterior areas; and (iii) the
mandibles of the male with three teeth, of which the apical and
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 4. Larva of Cyatta abscondita. (A) Lateral view. (B) Ventral view. (C) Head, dorsal view. (D) Head, anteroventral view. (E)
Anchor-tipped hairs on dorsum. (F) Anal region (white arrows indicate setal sockets; ventral at top).
doi: 10.1371/journal.pone.0080498.g004
worker and gyne of Cyatta differ from members of the neoattine
clade by (v) the node of the petiole well developed, high
(Figures 1c,d, 2a).
Most notably, Cyatta differs from all other attine genera and
species by the following autapomorphies: (i) mandible of the
worker and gyne with four teeth (Figures 1b, 2c); (ii) in ventral
view, metapleura of the worker and gyne with two spiniform
dorsal and lateral body hairs present and abundant, shared
with Mycocepurus species; (ii) a single seta present laterad of
the maxillary palp, shared with Mycocepurus species; (iii)
supra-antennal setae present and abundant, shared with
Mycocepurus goeldii; (iv) genal lobes absent, shared with the
paleoattines and the neoattine genus Mycetarotes. Larval
characters are unstudied in Kalathomyrmex. In addition, the
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Cyatta: A New Genus of Fungus-Farming Ants
Natural history
processes between the mid and hind coxae, apparently absent
in the male; (iii) apical margin of the pygidium medially
emarginate, V-shaped (Figures 2e,f); and (iv) forewing of the
male with a closed discal cell (Figure 3d).
Based on the extreme degree of morphological divergence
and the results of the divergence dating analyses (see below),
we have chosen to describe Cyatta as a new genus rather than
to describe it as a species within the genus Kalathomyrmex.
Discovery history. In 2003, a single stray worker of C.
abscondita was taken in a pitfall trap as part of an ant survey
conducted at the Reserva Particular do Patrimônio Natural
Serra das Almas, Crateús, CE, Brazil, a relatively undisturbed
area of Caatinga, a biome characterized by deciduous thorny
woodland vegetation [106]. The specimen was deposited in the
MZSP ant collection, where it was at first associated with the
Mycetophylax species group, but subsequently recognized as a
new neoattine genus by CK and CRFB. This isolated specimen
inspired the first attempt to locate C. abscondita in the field in
Serra das Almas in 2009 by CRFB and RMF. Unfortunately, it
was the end of the rainy season and the soil was covered by a
dense layer of grass, impairing observations of all small and
inconspicuous ants. Visual searching and leaf-litter extraction
failed to locate additional specimens, as did subsequent
surveys at the same locality.
In 2008, two workers were taken in pitfall traps in the Instituto
Brasileiro de Geografia e Estatística (IBGE) Cerrado preserve,
near FAL in Brasília, DF, Brazil. These specimens, deposited in
the MZSP, inspired attempts by JSC, TRS, CTL, and HLV to
locate the species at this locality beginning in 2009. The first
such attempt yielded only the collection of a series of stray
workers and an unsuccessful nest excavation; however,
subsequent visits resulted in the excavations of multiple nests
and collections of gynes, larvae, and cultivated fungi.
The only known male of the species was fortuitously
collected in 2011 by CR and MB when they accidentally
encountered two nests of C. abscondita while excavating a
nest of Mycocepurus goeldii in the Broa Preserve, Itirapina, SP,
Brazil.
The earliest known collection of C. abscondita was that of a
stray worker taken in a leaf-litter sample in Paineiras, MG, in
1999, only recently discovered in the entomological collection
at MZSP and recognized as belonging to this species. Most
recently, in 2011, two workers of C. abscondita were recovered
from pitfall traps in fragments of semideciduous forests in the
Sales and Pindorama municipalities in northwestern São Paulo
state. This history of discovery indicates that C. abscondita is
rarely collected by traditional methods. The cryptic nature of
foragers and of nest entrances makes it almost invisible to
traditional hand collecting. The rarity of individuals in pitfall and
leaf-litter samples remains puzzling, since the concentrations of
nests encountered at FAL and Broa Preserve suggest that it is
locally abundant. Now that the genus and species are
recognized and described, we hope that additional specimens
will be identified in unsorted material in collections as well as in
newly collected material from ant surveys in Brazil and perhaps
even elsewhere in South America.
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Macrohabitat
Most collections of C. abscondita are from Cerrado localities
(Figure 5). These include Fazenda Água Limpa (FAL) near
Brasília, the Broa preserve in São Paulo, the IBGE Cerrado
preserve in Brasília, DF, the Fazenda Olho D’Água in
Paineiras, MG, and the Reserva Particular do Patrimônio
Natural (RPPN) do Acangau in Paracatu, MG, all of which are
characterized by diverse Cerrado phytophysiognomies, ranging
from campo limpo to Cerrado sensu stricto [107]. The
predominant habitat, Cerrado sensu stricto, is a low canopy
arboreal woodland that is characterized by the presence of
small trees with a canopy height of less than 7 meters, shrubs,
and abundant ground vegetation [108–110]. Cerrado soil is
typically a red-yellow latosol, largely composed of well-drained
and nutrient-poor quartz sand with moderate clay content
below 15% [107,111]. Both FAL and Broa have typical Cerrado
climates with a marked dry season from May to September and
with a mean annual temperature and precipitation of 23°C and
~1420 mm, respectively [110]. For a complete account of
vegetation and soil compositions at FAL and Broa, see [112]
and [113]. The label data associated with the C. abscondita
worker from Fazenda Olho D’Água indicates that it was
obtained from a leaf-litter sample from a Winkler extractor. This
suggests that this worker was likely taken in either a riparian
forest or in “Cerradão,” because it is in such areas that trees
are dense enough to produce conspicuous accumulations of
leaf litter.
Some specimens of C. abscondita have been taken outside
the Cerrado biome (Figure 5). Most notably, a stray worker was
recovered from a pitfall sample taken in 2003 in a relatively
undisturbed area of Caatinga, a biome characterized by
deciduous thorny woodland vegetation [106], in the RPPN
Serra das Almas, Crateús, CE, Brazil. More recently, in 2011,
two workers of Cyatta abscondita were taken in pitfall traps in
fragments of semideciduous forests in northwestern São Paulo
state. This region is considered a transition zone between
Cerrado and endangered coastal Atlantic Forest [114].
Microhabitat.
Four nests of Cyatta abscondita were
excavated at FAL and two nests at Broa (summarized in Table
1). Nest entrances of four additional nests were located at FAL;
however, attempted excavations of these nests failed. At FAL,
seven of the excavated nests occurred on the side of a littleused dirt service road in Cerrado sensu stricto (Figure 6b) and
the eighth (nest 1, Table 1) on the lawn of the FAL dormitories
(Figure 6a). The roadside nests were directly exposed to
sunlight for most of the day, whereas the lawn nest was
shaded by the adjacent building in the morning and afternoon.
At the Broa preserve, both nests occurred in the shade of trees
in Cerrado sensu stricto. Both Broa colonies were excavated
serendipitously during excavations of Mycocepurus goeldii
nests and the C. abscondita nest entrances were not observed.
Foraging behavior. Foraging workers of Cyatta abscondita
are difficult to locate because colony sizes are small, workers
forage individually, and individuals are very small and cryptic
(Figure 6c). In mid-September, which coincides with the
beginning of the rainy season at FAL, three to four individuals
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 5. Known distribution of Cyatta abscondita.
doi: 10.1371/journal.pone.0080498.g005
five FAL nests, including nests 1 and 2 (Table 1), were likewise
observed foraging individually only after sunset. Only in the
case of FAL nest 1 were workers observed to forage in the
from three different nests, including nests 3 and 4 (Table 1),
were observed foraging at night between 22h and 23h. In
February and April, at the end of the rainy season, ants from
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 6. Habitat of Cyatta abscondita. (A, B) Fazenda Agua Limpa (FAZ). (A) Excavation of nest JSC100412-01 in dormitory
garden area. (B) Cerrado senso stricto, where colonies were found on the side of the road. (C,D) Nest entrance of Cyatta
abscondita (white arrows). (C) Worker entering nest. (D) Nest entrance of Cyatta abscondita, consisting of an inconspicuous ~1mm
diameter hole in the ground. (E) Chamber with pendant fungus garden. (F) Excavation of nest 4 (JSC110920-01). Black bars
indicate two chambers, the lower one 104 cm below the surface.
doi: 10.1371/journal.pone.0080498.g006
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Cyatta: A New Genus of Fungus-Farming Ants
escaped into adjacent tunnels. In each of the three queenright
nests (nests 2, 3, and 4), a single gyne was consistently
encountered in the deepest chamber (see Table 1); however,
additional chambers may have been present at greater depths,
because excavations were generally terminated upon
encountering the gyne. Brood was found only in FAL nest 4,
which was collected in September, the beginning of the rainy
season, suggesting that colonies of Cyatta abscondita reduce
their reproductive activities during the dry season. The
maximum number of workers encountered in colonies ranged
from ~20 (FAL nest 4) to 26 (Broa nest 5). One male was
collected in nest 5 at Broa on 21 July.
Garden morphology. Gardens were pendant and arranged
in filamentous curtains suspended from the chamber ceiling
(Figure 5e), similar to the fungus gardens of Mycocepurus
species [70,93,115,116] and of Kalathomyrmex emeryi (TRS,
JSC, pers. obs.). Single fungal curtains were 5–6 mm long and
1–2 mm wide and a maximum number of 50 curtains were
found in a single chamber. Curtains were directly attached to
the soil of the chamber ceiling rather than to rootlets. In nest 4,
which was maintained in laboratory culture for three months,
workers attached garden filaments to the plastic ceiling of the
nest box and cultivated suspended gardens. The filaments
were firmly attached to the plastic ceiling by an unknown
mechanism.
Phylogeny. Results of molecular phylogenetic analyses
incorporating four nuclear gene sequences from Cyatta
abscondita confirm the previous finding [95] that the tribe Attini
is divided by an ancient divergence into two major clades, the
Paleoattini and the Neoattini (Figure 7). Cyatta abscondita
occupies a relatively isolated position in the latter clade,
distantly related to the monotypic genus Kalathomyrmex
Klingenberg & Brandão, the result of an early divergence in the
Neoattini. Its phylogenetic position, nested well within the
paraphyletic group of "lower attine ants," strongly supports the
hypothesis that C. abscondita practices "lower attine
agriculture" [58].
A relaxed-clock-divergence dating analysis conducted in
BEAST using the Bayesian uncorrelated lognormal approach
with a normal prior on the root node (as described in Schultz &
Brady [95]), resulted in a chronogram in which Cyatta occupies
a position identical to that in the MrBayes results shown in
Figure 7. The BEAST chronogram indicates that Cyatta and
Kalathomyrmex diverged 26 Ma (95% CI= 18–34) and that the
earliest possible divergence of the clade (Cyatta +
Kalathomyrmex) from the rest of the Neoattini occurred 44 Ma
(95% CI= 37–51).
early afternoon on two consecutive days in April between 13h
and 15h during a time when the nest entrance was shaded
from direct sunlight. Unlike the other nests, nest 1 occurred in a
well-watered, human-managed grassy lawn. Nests 5 and 6
(Table 1), which were collected in July at the height of the dry
season at the Broa preserve in São Paulo State, were located
in the shade and, unfortunately, neither foraging nor nestbuilding activity was observed.
The entrance of one FAL nest (JSC090223-26) was located
~4.5 centimeters from the entrance of an adjacent
Mycocepurus goeldii nest. At around 23h a Cyatta abscondita
worker was observed lurking slightly inside the nest entrance
while workers of M. goeldii foraged on bait (granules of Cream
of Rice cereal) placed near the nest entrances. When M.
goeldii workers were absent, the C. abscondita worker darted
out to retrieve a piece of bait and quickly returned to its nest.
This lurking and rapid foraging behavior was repeated until the
supply of bait was depleted. In rare cases of contact between
C. abscondita and M. goeldii workers, C. abscondita workers
were observed to remain motionless. Aggressive interactions
were not observed.
Nest architecture. At FAL, nest entrances of Cyatta
abscondita consisted of a single, inconspicuous, hole in the
ground of approximately 1 mm in diameter without any
accompanying mound or turret (Figures 6c,d). As mentioned
above, the entrance of one nest was located in the mound of a
Mycocepurus goeldii colony ~4.5 cm from the M. goeldii nest
entrance. At the Broa preserve, nest chambers of C.
abscondita were encountered serendipitously while excavating
M. goeldii nests and the nest entrances were not observed.
At FAL, excavations of eight nests were attempted. Four
excavations (JSC090223-26, JSC110914-02, JSC100415-03,
JSC100416-04) failed (i.e., neither chambers containing fungus
gardens nor gynes were found, but workers were collected at
their respective nest entrances), but chambers containing
fungus gardens were located in four nests (Table 1). Nests
contained three to eight chambers. In FAL nests 1 and 3, which
contained 4 and 3 chambers respectively, chambers were
roughly arranged vertically below the nest entrance (Table 1),
although it is possible that additional, laterally dispersed
chambers were missed during the excavations. At FAL, nests 2
and 4 contained 7 and 8 chambers, respectively, some of
which occurred at the same depth but were laterally separated
from each other (Figure 6f). The shallowest chamber
encountered (nest 3, FAL) was 29 cm deep and the deepest
chamber (nest 6, Broa) was 195 cm deep. Because no gynes
were found during the nest excavation at Broa, it is entirely
possible that additional chambers occurred below a depth of 2
meters. Chambers were elliptically shaped, 1–2.5 cm wide and
2–5 cm high (Figure 6e). The largest garden chamber
encountered (nest 2, FAL) was 2.5 x 5.5 cm; at Broa, a
similarly sized chamber (nest 5) contained ~50 hanging garden
filaments (Figure 6e). Some chambers were empty; in one
case, an empty chamber contained three polydesmid
millipedes.
Demography. Dealate gynes were collected in three of the
eight excavated nests, suggesting that in five nests additional
chambers remained undiscovered in the soil, or that gynes
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Discussion
The pursuit and discovery of phylogenetically informative
new species are arguably among the most important
enterprises in systematic biology. Numerous studies have
demonstrated the significant effects of taxon representation on
phylogenetic inference, including, in addition to tree topology,
ancestral character state reconstruction, divergence time
estimation, and inferences of evolutionary rates [117–119].
Ward et al. [118] showed that the exclusion of a single relict
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Cyatta: A New Genus of Fungus-Farming Ants
Figure 7. Phylogenetic position of Cyatta abscondita. This phylogeny of 66 fungus-farming and 26 outgroup ant species results
from a Bayesian analysis of four nuclear protein-coding genes (see text for details). Fungus-farming ant species are indicated by
bold black branches; the branch subtending Cyatta abscondita is indicated in red. Gray branches correspond to non-fungus-farming
taxa. Blue dots on branches represent Bayesian posterior probabilities of 100; orange dots represent Bayesian posterior
probabilities of 95–99. Divergence time of Cyatta and Kalathomyrmex estimated at 26 Ma (95% CI= 18–34) and divergence of the
clade (Cyatta + Kalathomyrmex) from the rest of the Neoattini estimated at 44 Ma (95% CI= 37–51).
doi: 10.1371/journal.pone.0080498.g007
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Cyatta: A New Genus of Fungus-Farming Ants
species resulted in the incorrect reconstruction of the
phylogeny of the ant subfamily Dolichoderinae (Formicidae). In
addition, the recently discovered ant genus Martialis, a relict
subterranean species known from the Amazon forest in Brazil,
has been shown to be the only hitherto known representative of
an early diverging branch of the ant tree of life [27]. Within the
Attini, the recently described ant genus Mycetagroicus
[105,120] was found to be the sister group to the higher attine
ants (Sericomyrmex, Trachymyrmex, Acromyrmex, and Atta)
and thus to occupy a phylogenetic position transitional between
lower and higher agriculture [95]; however, until very recently
its fungal cultivar association remained unknown. Subsequent
field work documented that Mycetagroicus cerradensis
cultivates a lower attine fungus, suggesting that biological
investigations of the genus are critical for understanding the
evolutionary transition from lower to higher agriculture [94].
This strategy of reciprocal illumination (i.e., information
gathered from the field informing phylogenies, and phylogenies
guiding field work) plays a key role for reconstructing and
understanding the macro- and micro-evolutionary processes
driving the attine agricultural symbiosis.
The results reported here indicate that Cyatta abscondita
possesses an intriguing mosaic of characters, some that are
shared with paleoattines, others that are shared with
neoattines, and at least one that is shared only with non-attine
ants. Because the Neoattini, Paleoattini, and the non-attine
Myrmicinae span the ancestral node of the tribe Attini, this
combination of character states suggests that the morphology,
behavior, fungal associations, nest architecture, and other
biological characters of C. abscondita are potentially
informative about plesiomorphic character states within the
tribe and, consequently, about the early evolution of ant
agriculture.
At least one character of C. abscondita, the presence of a
closed discal cell in the forewing of the male, is unknown in all
other Attini. If, as we suspect, this is a retained plesiomorphy
rather than an autoapomorphy, then the absence of the discal
cell in other Attini must be the result of at least three parallel
losses, one in the Paleoattini, one in the Neoattini, and one in
Kalathomyrmex.
Another character previously unknown in the Attini is the
presence of at least two rows of elongate anchor-tipped hairs
(Figures 4a,e) on the mid-dorsum of the larva. The function of
such anchor-tipped hairs has recently been studied in the nonfungus-farming ant Pheidole rhea, which utilizes these
specialized setae to hang fourth-instar larvae from the nest
walls [121]. The widespread presence of this character state in
non-fungus-farming ants strongly suggests that it is
plesiomorphic for the Attini and that its presumably derived
absence in most Attini may be connected to the fact that larvae
are usually more or less enveloped in mycelium deep within the
fungus garden rather than hung from the chamber wall.
Presumed plesiomorphic adult character states shared by C.
abscondita and the Paleoattini include the presence of a
rounded inferior lateral margin of the pronotum, also retained in
Kalathomyrmex emeryi. All other neoattine genera, from
Mycetarotes to the leaf-cutter ants, have a denticle or tooth in
this position. A number of larval character states are shared
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with species of the paleoattine genus Mycocepurus, including
the presence of dorsal and lateral hairs, the presence of a
single seta laterad of the maxillary palp, and abundant supraantennal setae. The absence of genal lobes is shared with all
Paleoattini as well as, in the Neoattini, with Mycetarotes
species. (Larval characters of Kalathomyrmex have not yet
been documented.) The striking pendant, curtain-like
morphology of the fungus garden is a character state shared
with Mycocepurus species as well as with Kalathomyrmex.
Presumed neoattine synapomorphies shared by C.
abscondita and other Neoattini include, in adults, (i) the lack of
hypostomal teeth, also secondarily lost in some species of
Apterostigma; (ii) the antennal funicular segment II of males
short, as long as or slightly longer than funicular segment I
(pedicel), whereas in the males of the paleoattine genera the
funicular segment II is long, almost twice as long than the
pedicel; and (iii) the wide separation of the maxillary palp from
the galea in the larvae.
Although both molecular and morphological data indicate
that Cyatta abscondita is the sister species of Kalathomyrmex
emeryi, it is a very distant sister, having diverged from their
most recent common ancestor approximately 26 mya. As far as
is currently known, C. abscondita shares with Kalathomyrmex
two unique morphological characters, the form of the clypeus
and the morphology of the mandibles in the male. In common
with the paleoattines, but differing from all other neoattines, C.
abscondita also shares with Kalathomyrmex a rounded inferior
pronotal corner. In contrast to these shared character states,
two synapomorphic and one symplesiomorphic, C. abscondita
notably lacks the defining feature of Kalathomyrmex, the
basket-like psammophore (Gr. kalathos = "basket") and differs
not only from Kalathomyrmex but from all other Attini in a
number of striking characters, including the 4-toothed
mandible, the presence of paired ventral pleural spiniform
processes, and the presence of a discal cell in the wing of the
male. In fact, the morphology of C. abscondita is a mosaic of
characters of the paleoattine and neoattine clades as well as of
closely related non-attine myrmicines. For these reasons we
choose to recognize Cyatta abscondita as a distinct genus
within the fungus-farming ants.
The discovery, description, and mapping of biological
diversity is essential for devising strategies for protecting
biodiversity hotspots, i.e., areas that support high
concentrations of endemic species and that are threatened due
to the rapid loss of habitat as a result of years of unsustainable
human exploitation [86], [122]. The Brazilian Cerrado is one
such biodiversity hotspot. With only 20% of the original primary
habitat remaining, and with only 6.2% of that habitat protected,
the Brazilian Cerrado sustains more than four thousand
species of endemic plants and more than a hundred species of
endemic vertebrates [86]. The Caatinga is even less protected
than the Cerrado [123]. The discovery of Cyatta abscondita in
the Cerrado and in the poorly explored Caatinga habitats of
Brazil suggests that increasing the search for cryptic and
inconspicuous species will lead to discoveries that will
fundamentally alter our understanding of insect evolutionary
history.
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Cyatta: A New Genus of Fungus-Farming Ants
Acknowledgements
are thankful to Fundação Acangau for granting permission to
HLV to collect at RPPN Acangu. We thank Scott Whittaker
(NMNH) for help with preparation of the larvae, Ms. Jessica
Louton and Dr. Natasha Mehdiabadi (NMNH) for help with
molecular work, Dr. Sean Brady (NMNH) for help with dating
analyses, Ms Claudia Ortiz (Universidad Nacional de
Colombia) for help with ArcGIS, and Ms. Eugenia Okonski
(NMNH) for help with specimen preparation.
We thank the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) and the Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA)
for permission to conduct fieldwork in Brazil (permit numbers
14789–1, 14789–3). We are extremely grateful to two
anonymous reviewers for providing thoughtful and constructive
suggestions and comments. The manuscript is much improved
as a result. Thanks to Dr. Yves P. Quinet and Francyregis
Nunes for allowing us to study the only known specimen from
the Caatinga and for the support to CRFB and RMF during field
work in Crateús. We thank Dr. Rogerio R. Silva for calling our
attention to the São Paulo specimens. We are indebted to Dr.
Helena C. Morais (Universidade de Brasília), Dr. Karen
Camargo (CNPq), and Jonas Maravalhas (UFU) for logistics
during our work in Brasília and FAL and to Prof. José Mauro da
Silva Diogo (FAL Director) for permission to work at FAL. We
Author Contributions
Conceived and designed the experiments: JSC TRS CRFB CK
RMF CR MB CTL HLV. Performed the experiments: JSC TRS
CRFB RMF CR CTL MB. Analyzed the data: JSC TRS CRFB
RMF CR. Contributed reagents/materials/analysis tools: JSC
TRS CRFB CK RMF CR MB CTL HLV. Wrote the manuscript:
JSC TRS CRFB CK RMF CR MB CTL HLV. Obtained
permissions for collecting specimens: HLV MB CRFB.
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