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© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20 1
Zoological Journal of the Linnean Society, 2020, XX, 1–20. With 8 figures.
The first known riodinid ‘cuckoo’ butterfly reveals
deep-time convergence and parallelism in ant social
parasites
LUCAS A. KAMINSKI1,*,, LUIS VOLKMANN2, CURTIS J. CALLAGHAN3,
PHILIP J. DEVRIES4, and ROGER VILA5
1Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul
(UFRGS), Porto Alegre, Rio Grande do Sul, Brazil
2Ecosistemas Argentinos, Los Cocos, Córdoba, Argentina
3Casa Picapau, Floresta de la Sabana, Bogotá, Colombia
4Department of Biological Sciences, University of New Orleans, New Orleans, LA, USA
5Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
Received 15 April 2020; revised 30 September 2020; accepted for publication 17 October 2020
Mutualistic interactions between butterflies and ants can evolve into complex social parasitism. ‘Cuckoo’ caterpillars,
known only in the Lycaenidae, use multimodal mimetic traits to achieve social integration into ant societies. Here, we
present the first known ‘cuckoo’ butterfly in the family Riodinidae. Aricoris arenarum remained in taxonomic limbo for
> 80 years, relegated to nomen dubium and misidentified as Aricoris gauchoana. We located lost type material, designated
lectotypes and documented the morphology and natural history of the immature stages. The multifaceted life cycle of
A. arenarum can be summarized in three phases: (1) females lay eggs close to honeydew-producing hemipterans tended by
specific Camponotus ants; (2) free-living caterpillars feed on liquids (honeydew and ant regurgitations); and (3) from the
third instar onward, the caterpillars are fed and tended by ants as ‘cuckoos’ inside the ant nest. This life cycle is remarkably
similar to that of the Asian lycaenid Niphanda fusca, despite divergence 90 Mya. Comparable eco-evolutionary pathways
resulted in a suite of ecomorphological homoplasies through the ontogeny. This study shows that convergent interactions
can be more important than phylogenetic proximity in shaping functional traits of social parasites.
ADDITIONAL KEYWORDS: ant-organs – convergent interactions – exploitation of mutualism – kleptoparasitism
– Lemoniadina – Nymphidiini – symbiosis – tactile mimicry.
INTRODUCTION
Trophobiotic interactions between caterpillars and
ants, termed myrmecophily, occur widely in two families
of butterflies (Lycaenidae and Riodinidae; reviewed by
DeVries, 1991b; Fiedler, 1991; Pierce et al., 2002). In
general, these interactions are considered mutualistic
and are mediated by specialized larval ant-organs that
produce substrate-borne vibrations, chemical signals and
nutritional rewards for ants, whereas ants can provide
protection against natural enemies (e.g. Pierce & Mead,
1981; DeVries, 1991a). From the free-living ancestral
strategy (commensalism or mutualism) on plants, social
parasitism can evolve, when the caterpillars begin to
exploit the resources of the ant colony (Cottrell, 1984;
Pierce & Young, 1986; Fiedler, 1998). An iconic example
of this parasitic lifestyle is provided by the large blue
butterfly, Phengaris Doherty, 1891 (= Maculinea Van
Eecke, 1915), which parasitizes Myrmica Latreille,
1804 (Myrmicinae) ant colonies in Europe and Asia
(Als et al., 2004; Casacci et al., 2019). Inside the ant
nest, Phengaris caterpillars exploit ant resources
either by predation on the ant brood (carnivory) or via
a ‘cuckoo’ strategy, a type of kleptoparasitism in which
caterpillars are fed directly by ants with regurgitations
(trophallaxis) (Thomas & Wardlaw, 1992). Although
rare, there are other known cases of social parasitism
in Lycaenidae from Eurasia, Africa and Australia (e.g.
Cottrell, 1984; Pierce, 1995; Fiedler, 1998; Heath, 2014).
There is no confirmed case of social parasitism on the
*Corresponding author. E-mail: lucaskaminski@yahoo.com.br
applyparastyle “fig//caption/p[1]” parastyle “FigCapt”
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2 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
American continent (Fiedler, 2012), in the Lycaenidae
or in the sister family Riodinidae, a mainly Neotropical
lineage (DeVries, 1997).
In Riodinidae, a candidate group to contain social
parasitic species is Aricoris Westwood, 1851, a
Neotropical genus, previously referred to as Hamearis
Hübner, 1816 and Audre Hemming, 1934 (Hall &
Harvey, 2002), which contains few anecdotal reports
of caterpillars found in ant nests (Bruch, 1926;
Bourquin, 1953; DeVries et al., 1994; DeVries, 1997).
In the first detailed description of a myrmecophilous
larva of Riodinidae, Bruch (1926) reports that larvae
of Aricoris signata (Stichel, 1910) were found inside
Solenopsis Westwood, 1840 (Myrmicinae) ant nests.
Although the larvae were found together with ants,
A. signata larvae are phytophagous and apparently
do not receive a food resource from the ants, i.e. this
species is not a true social parasite (Fiedler, 2012). The
same type of behaviour was observed in the closely
related species Aricoris propitia (Stichel, 1910), whose
caterpillars rest during the day inside underground
shelters constructed by tending ants (Kaminski &
Carvalho-Filho, 2012). Other observations of Aricoris
larvae in ant nests were made by DeVries et al. (1994),
who recorded two species (cited as ‘Audre nr. aurinia’
and ‘undetermined sp.’) inhabiting Camponotus
Mayr, 1861 (Formicinae) ant nests in Jujuy, northern
Argentina. In contrast to the observations on A. signata
and A. propitia, the caterpillars were not phytophagous
and did not accept any type of solid food item in the
laboratory, suggesting that the larvae might feed via
ant trophallaxis (DeVries et al., 1994; DeVries, 1997).
Callaghan (2010) reported the observation of fresh
adults of Aricoris tutana (Godart, 1824) emerging from
an ant nest in Central Brazil and suggested that larvae
might feed on ant resources. Thus, only circumstantial
evidence of social parasitism in Riodinidae has existed
so far (DeVries et al., 1994; Gallard, 2017).
In this study, we describe the life cycle of a
kleptoparasitic species of Aricoris from South America
and thus confirm that this strategy also evolved in
Riodinidae, which until now was regarded as an exclusive
strategy of the family Lycaenidae (Fiedler, 2012). This
study began with observations by Volkmann & Núñez-
Bustos (2010), who reported Aricoris gauchoana (Stichel,
1910) caterpillars feeding on exudations of scale insects
and suggested that caterpillars could complete their life
cycle inside the ant nest. After comparison of immature
and adult specimens, we conclude that the species
identified as A. gauchoana by Volkmann & Núñez-
Bustos (2010) is the same species reported by DeVries
et al. (1994) as Audre nr. aurinia and later cited as
Audre aurinia Hewitson, 1863 by Pierce (1995) and as
Aricoris incana (Stichel, 1910) by Hall & Harvey (2002).
Through the examination of the literature and museum
collections, we show that this kleptoparasitic species is
not represented by the name A. gauchoana, but by the
obscure name Hamearis arenarum H. Schneider, 1937
from Uruguay and currently relegated to anonymity as
a nomen dubium (Hall & Harvey, 2002; Callaghan &
Lamas, 2004; Siewert et al., 2014a). Thus, the purposes of
this article are as follows: (1) to confirm the first instance
of ‘cuckoo’ caterpillars in Riodinidae; (2) to elucidate the
status of this taxon, redescribing the species Aricoris
arenarum (Schneider, 1937) and designating lectotypes;
(3) to describe their immature morphology and natural
history; and (4) to discuss convergence and parallelism
between the families Lycaenidae and Riodinidae, thus
contributing new perspectives on the evolution of social
parasitism in butterflies.
MATERIAL AND METHODS
Study sites, behavioural observation and
collection
The fieldwork was conducted in areas of montane ‘chaco’
vegetation in Capilla del Monte (30°52′S, 64°32′W, 985 m
a.s.l.), San Ignacio (30°56′S, 64°31′W, 1053 m a.s.l.) and
Villa Giardino (31°3′S, 64°29′W, 1050 m a.s.l.) and high-
elevation grasslands in La Cumbre (30°56′S, 64°23′W,
1400 m a.s.l.), Córdoba, Central Argentina. These
populations were monitored over several years by L.V.
(see Volkmann & Núñez-Bustos, 2010) and studied in
detail in the summer months (January and February)
of 2013–2019 by L.V. and L.A.K. The behaviour of
adults and caterpillars (early instars) was observed ad
libitum (sensu Altmann, 1974) in the field during the
day (~10.00–17.00 h) and night (~22.00–02.00 h). Host
plant branches containing early instars, honeydew-
producing Hemiptera and tending ants were collected,
maintained in plastic pots (~500 mL) and observed
with a stereomicroscope in the laboratory. Additionally,
a ‘black morph’ colony of Camponotus punctulatus
Mayr, 1868 (Formicinae) from San Ignacio was collected
that contained brood chambers with immature and
adult ants of all castes. The ant nest was kept in the
laboratory and fed weekly with honey and insects. After
2 days to stabilize the colony, we inserted two third
instar A. arenarum caterpillars, which were monitored
until the end of their development. These observations
were complemented with data obtained by P.J.D. in
April 1992 in Volcán (23°59′S, 65°27′W, 1800 m a.s.l.),
Jujuy, Argentina; and by L.A.K. and L.V. in January
2020 in Castillos (33°49′S, 57°40′W, 90 m a.s.l.), Soriano,
Uruguay. Plants with immatures, in addition to tending
ants, were collected for identification. Immatures for
morphological analysis were fixed in Dietrich’s solution
and preserved in 70% ethanol. Shed head capsules were
collected and preserved for measurement. Vouchers
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 3
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
of tending ants, hemipterans and immature stages
were deposited at the Departamento de Zoologia,
Universidade Federal do Rio Grande do Sul (UFRGS),
Porto Alegre, Rio Grande do Sul, Brazil.
Morphology
Morphological examination and measurements were
made using a stereomicroscope (Nikon AZ100M). To
study the genitalia, dissections were made according
to the standard practice of soaking the abdomens in
10% KOH overnight or heating in a bain-marie for
5–10 min and storing the pelts and genitalia in glycerol.
Wings for the study of venation and appendages were
detached, soaked briefly in bleach, then washed in
alcohol and mounted on slides. Egg size is given as
height and diameter. Larval head capsule width was
measured as the distance between the most external
stemmata, and the maximum length for both larvae
and pupae correspond to the distance from the head
to the posterior margin of the abdominal segment
in dorsal view. Measurements are given as a range.
Colour patterns of immature stages were recorded
using a digital camera in vivo, and a stereomicroscope
was used for eggs and early instars. Scanning electron
microscopy (SEM) was conducted using a JEOL JSM-
6060 microscope, with samples prepared according to
standard techniques (for details, see Kaminski et al.,
2012). The terminology of the genitalia follows Klots
(1970) and that of the venation follows Miller (1970).
The taxonomic status of the names is based on the
study by Callaghan & Lamas (2004). We follow Downey
& Allyn (1980) for egg morphology, Stehr (1987) for the
general morphology of larvae and pupae, and Cottrell
(1984) and DeVries (1988) for ant-organs.
The studied material belongs to the following
collections: CAM, Coleção Alfred Moser, São Leopoldo,
Rio Grande do Sul, Brazil; CENB, Collection Ezequiel
Núnez-Bustos, Buenos Aires, Argentina; CJC, Curtis
Callaghan Collection, Bogotá, Colombia; CLK, Coleção
Lucas Kaminski, Porto Alegre, Rio Grande do Sul,
Brazil; DZRS, Departamento e Zoologia, Universidade
Federal do Rio Grande do Sul, Porto Alegre, Rio
Grande do Sul, Brazil; DZUP, Departamento de
Zoologia, Universidade Federal do Paraná, Curitiba,
Paraná, Brazil; FCE, Collection the Facultad de
Ciencias, Universidad de la República (UDELAR),
Montevideo, Uruguay; IML, Instituto Miguel Lillo,
San Miguel de Tucumán, Tucumán, Argentina; MCZ,
Museum of Comparative Zoology, Harvard University,
Boston, MA, USA; MfN, Museum für Naturkunde,
Berlin, Germany; MLP, Museo de La Plata, La
Plata, Argentina; MNHNPA, Museu Nacional de
Historia Natural, Asunción, Paraguay; MNRJ, Museu
Nacional da Universidade Federal do Rio de Janeiro,
Rio de Janeiro, Brazil; NHMUK, Natural History
Museum, London, UK; OM, Coleção Olaf Hermann
Hendrik Mielke, Curitiba, Paraná, Brazil; SFN,
Senckenberg Research Institute and Natural History
Museum Frankfurt, Frankfurt am Main, Germany;
ZfB, Zentrum für Biodokumentation, Schiffweiler,
Saarland, Germany. Abbreviations used throughout
the text are as follows: DFW, dorsal forewing; DHW,
dorsal hindwing; FW, forewing; HW, hindwing; PCO,
perforated cupola organ; TNO, tentacle nectary organ;
VFW, ventral forewing; VHW, ventral hindwing.
evolutionary coMparison with social
parasitisM in lycaenidae
The life cycle of A. arenarum was compared with
that known for lycaenids and classified according to
the system proposed by Fiedler (1998). Based on this
classification, we decided to compare the ecological and
morphological traits of A. arenarum in detail with those
of Niphanda fusca (Bremer & Grey, 1853) (Lycaenidae:
Polyommatinae), a social parasite with a similar life
cycle. To demonstrate the evolutionary relationship
between A. arenarum and N. fusca, the age of
divergence and estimated origins of myrmecophily,
we used the dated phylogenomic hypothesis proposed
by Espeland et al. (2018). The systematic position of
A. arenarum was deduced from morphological and
molecular evidence (Hall & Harvey, 2002; Seraphim
et al., 2018). The life cycle of N. fusca has been inferred
based on the documentary ‘Relationships in Nature’
(MBC TV, Republic of Korea, available at: https://www.
youtube.com/watch?v=Qc8LDIIpnTA), photographs
posted in the ‘Ant Room’ blog (available at: http://blog.
livedoor.jp/antroom/) and the rich literature for this
well-studied model species (e.g. Nagayama, 1950; Hojo
et al., 2009, 2014). Owing to the taxonomic sampling
of the phylogeny of Espeland et al. (2018), which
collapses many important lineages of social parasitic
and non-parasitic lycaenids and subsamples relevant
riodinid linages, we prefer not to carry out a formal
character reconstruction analysis. This can be done
with the addition of new life-history data and a more
comprehensive phylogeny, ideally covering most of the
diversity in the subtribe Lemoniadina and in the genus
Aricoris in particular. Thus, as a first approach to identify
convergence and parallelism in traits and interactions
we used a simple comparative natural history method
from a phylogenetic perspective (Bittleston et al., 2016).
RESULTS
SysteMatics
History of classification
The subspecies Hamearis aurinia gauchoana Stichel,
1910 was described based on two female syntypes
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4 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
from Uruguay (Stichel, 1910). One female labelled
as Type from the Staudinger collection is at the MfN
(Fig. 1A). A male specimen was also found in the same
collection without a type or locality label, but with
a number (3557) and an identity label in Stichel’s
handwriting indicating ‘gauchoana Stichel’. However,
this male represents a different species, lacking the
prominent submarginal rows of spots on both wings
and with a nearly uniform grey ground colour on the
VHW. Comparison of the female type specimen with
Stichel’s description confirms this as a syntype of
H. a. gauchoana. However, in all the literature since
then, including widely used South American field
guides, the name gauchoana has been associated
erroneously with the male phenotype and not the
female (e.g. Hayward, 1973; Biezanko et al., 1978;
Canals, 2000, 2003; Hall & Harvey, 2002; Núñez-
Bustos, 2010; Volkmann & Núñez-Bustos, 2010;
Siewert et al., 2014b). Adults illustrated by D’Abrera
(1994) under the name ‘gauchoana’ are A. incana. The
name ‘gauchoana’ was always treated as a subspecies
of Aricoris aurinia and never separated formally as a
species until the study by Hall & Harvey (2002).
In 1937, H. Schneider described two riodinid species
from Uruguay: Hamearis arenarum and Hamearis
montana (as ‘montaña’ [sic]). Neither was illustrated,
nor were the type depositories indicated. Schneider’s
material is located at two German Institutions: the
SFN and the ZfB. Among the specimens at the SFN
were a male and female with labels in Schneider’s
distinctive handwriting indicating the type locality
of H. montana as Aiguá, [Maldonado department],
Uruguay. These specimens are on loan and are at
present in the Smithsonian Museum, Washington, DC,
USA (examined and cited by Hall & Harvey, 2002).
Photographs of those specimens are available at the
Butterflies of America website (Warren et al., 2016)
and fit Schneider’s description, suggesting that these
are indeed syntypes of that species (Hall & Harvey,
2002). Additional syntype specimens in the ZfB are:
two males, one from Aiguá and the other labelled
‘Uruguay’; and three females, two from the Sierra de
la Animas, Maldonado, Uruguay and another labelled
‘Uruguay’ (Fig. 1B). Comparison of Stichel’s female
syntype of H. a. gauchoana with Schneider’s female
syntype of H. montana indicates that they refer to the
same species (Fig. 1A–C); thus H. montana Schneider,
in addition to its junior subjective synonyms, Hamearis
erycina Schweizer & Kay, 1941 and Audre drucei
nordensis Callaghan, 2001, become junior subjective
synonyms of H. a. gauchoana.
In addition, one male (Fig. 1D) and one female
(Fig. 1E) were located at ZfB with labels in Schneider’s
handwriting with the name ‘Hamearis arenarum
Schneider, neue [new]’. Both specimens are from La
Barra, 29 November 1936. Both fit the description
of H. arenarum. The specimens referred to in the
description are one male and several females from
Rincón de la Bolsa, San José, Uruguay, currently
known as Ciudad del Plata. La Barra was located in
the same vicinity. Both localities are found near the
south coast of Uruguay in the Montevideo area, and
thus, the specimens can be considered as belonging
to the same population. From Schneider’s detailed
description, it is clear that H. arenarum refers to the
male (no. 3557) at the MfN, which Stichel labelled as
H. gauchoana. For instance, Schneider refers to the
VHW as being ‘uniform light grey with a row of small
black dots’ (our translation) (Figs 1D, E, 2A). Thus,
arenarum is the valid name for what has been referred
to in the literature as gauchoana.
The resulting synonymies for these two species are
as follows:
Aricoris gauchoana (Stichel, 1910)
= montana (Schneider, 1937), syn. nov. (Hamearis)
= erycina (Schweizer & Kay, 1941), syn. nov. (Hamearis)
= drucei nordensis (Callaghan, 2001) syn. nov. (Audre)
Aricoris arenarum (Schneider, 1937), (Hamearis)
= gauchoana Auctorum non Stichel, 1910
Aricoris ArenArum (schneider, 1937)
Hamearis arenarum Schneider, 1937: Entomologische
Rundschau 55(12): 137–138.
Type locality
La Barra, Uruguay. A male lectotype (ZfB), here
designated, has the following labels: /Atencion! selten
Hamearis arenarum Schneider [female symbol] Neue
Art / La Barra 29.xi.36 / LECTOTYPE Hamearis
arenarum Schneider, 1937 Callaghan & Kaminski det.
2020/. The characteristic lectotype label will be sent to
the curator of the collection.
Proposed common names
Brown patchwork (Canals, 2003), cuckoo metalmark
(English); colage parda (Canals, 2003), hormiguera
ocrácea (Volkmann & Núñez-Bustos, 2010), hormiguera
chopí (Spanish); formigueira chupim (Portuguese);
panambi chopi (Guarani).
Diagnosis
Despite historical confusion, A. arenarum and
A. gauchoana are easily differentiated by the wing
colour pattern (Fig. 1). However, some difficulty
might exist in distinguishing A. arenarum from other
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 5
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
Aricoris species, such as Aricoris aurinia and Aricoris
indistincta (Lathy, 1932), which also have a nearly solid
grey tone ventrally on the hindwing and the general
orange colour pattern dorsally. However, A. arenarum
can be identified externally by the median band of
spots on the VHW, in which, when visible, the spot in
cell M3 is displaced distally, aligned to that in cell M2.
Internally, A. arenarum male genitalia (Fig. 2B–D)
Figure 1. Adult types of Aricoris described from Uruguay. A, Hamearis gauchoana, holotype female in dorsal view (left),
ventral view (centre) and labels (right). B, Hamearis montana, lectotype male in dorsal view (left), ventral view (centre) and
labels (right). C, H. montana, female paralectotype in dorsal view (left), ventral view (centre) and labels (right). D, Hamearis
arenarum, lectotype male in dorsal view (left), ventral view (centre) and labels (right). E, H. arenarum, female paralectotype
in dorsal view (left), ventral view (centre) and labels (right). Scale bar: 1 cm.
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6 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
can be distinguished based on the presence of an
indentation in the valvae ventral edge, below the tip,
and because the two prongs of the eighth abdominal
sternite do not extend beyond the pleural membrane,
characters present also in the ‘chilensis’, ‘constantius’
and ‘colchis’ groups (sensu Hall & Harvey, 2002).
Figure 2. Adults of Aricoris arenarum. (A) In copula in Castillos, Uruguay, showing the female (left) and male (right); note
cryptic coloration on the ground. (B–F) Male (B–D) and female (E, F) genitalia of A. arenarum. B, lateral view. C, ventral
view. D, eighth sternite in ventral view. E, ventral view. F, papilla analis. Scale bar: 0.5 mm.
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 7
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
Redescription of adult morphology: male (Fig. 1D)
Average forewing length 16.6 mm, range 18–20 mm
(N = 6).
Wing shape and venation: FW with four radial veins; R1
and R2 branch before the discal cell. HW with humeral
vein long, curved, and 2A reaching the anal margin
before the midpoint. FW costa slightly indented before
a pointed apex; distal margin to tornus curved convex
to origin; inner margin slightly indented. HW costa
straight to Sc, then curved to a rounded apex at M1,
then curved abruptly to anal angle; the distal margin
slightly indented between Cu2 and 2A; inner margin
slightly concave to base.
Dorsal surface: Ground colour of discal area in wings
orange; limbal area black; base orange, variably
infused with black scaling. FW costa with grey-brown
scaling; discal cell with three large, irregular black
spots, with two similar spots below in cell Cu2; distad
an irregular post-discal band of white spots from cells
R2 to 2A, edged basad in black and variably infused
with orange scaling; the second middle spot offset
distally, the next two in cells M2 and M3 together, those
in cells Cu2 and 2A offset basally, all bordered basad
by black separating them from orange discal area;
distally a submarginal row of prominent rounded
yellow-orange spots; distad of this a marginal row of
small, indistinct orange/yellow spots; fringe black with
variable grey. HW costa with variable black; basal area
ground colour dark brown with an irregular central
yellow-orange band; post-discal area yellow-orange
enclosing an irregular postmedian band of small black
spots, with those in cells M2 and M3 offset distad;
limbal area orange containing a submarginal row of
black spots, one in each cell except Cu2 where there
are two, encircled with yellow-orange scaling; margin
black, fringe variably grey-brown.
Ventral surface: Ground colour of both wings variable
grey-brown. FW discal area with yellow-orange scaling
and three large orange spots outlined variably in black
and separated with white scaling; cell Sc with three
faint grey spots; cell Cu2 with two large black spots
separated with white; post-discal row of rounded white
spots bordered basally with black scaling, and distally
with black scaling from cell M2 to Cu2; submarginal row
of faint black spots surrounded by lighter scaling, grey
with some yellow-orange distad, margin grey; fringe
light grey-brown. HW discal area with dorsal figures
faintly outlined in dark grey; postmedian irregular row
of small dark spots, margin black, fringe grey-brown.
Head: Frons light brown; upper surface white. Labial
palpi 3.1 mm long; first two segments white, third
black and curved. Proboscis light brown; swollen at
base. Antennal length 60% of forewing length.
Body: Thorax and abdomen dark-brown dorsally;
collar light brown. Ventral surface and appendages
white. Forelegs truncated, with tibia and unimerous
tarsus slender and nearly same length; femur
shortened. Midlegs and hindlegs grey-brown, with long,
black spurs with scattered spines on inner margin of
tarsal segments. Abdomen black-brown dorsally, white
ventrally.
Genitalia (Fig. 2B–D; N = 5): Uncus widely separated
in ventral view. Socci high, triangular. Tegumen deeply
notched between leaves, basally rounded. Falces
pointed, turned inward. Vinculum curved from tegumen
to just before saccus, wide, supporting extension of
eighth sternite segment caudad. Valvae long, pointed,
indented ventrally before tip; rounded tips with three
or four socketed teeth; dorsally nearly flat. Aedeagus
curved, with long, pointed tip. Eighth sternite segment
(rami) narrow, curved outward, not joined at base or
extending beyond the plural membrane.
Redescription of adult morphology: female
(Fig. 1E)
Female (Fig. 1E): Forewing length 16.8 mm, range
18–21 mm (N = 5). The female differs from the male
as follows.
Wing shape: FW distal margin slightly more rounded
than male, with more rounded apex, costa straight;
otherwise the same.
Dorsal surface: Lighter ground colour and generally
greater width of the median band, in which the yellow-
orange spots are larger and joined.
Ventral surface: Lighter than male; ground colour
of both wings grey. FW row of white spots wider
than dorsal and continuous. On HW, markings less
prominent.
Head: Smaller than the male. Proboscis is narrow and
light brown.
Body: Same colour as male. Forelegs more elongated
than in males; mid- and hindlegs have fewer spines
and no black spurs.
Genitalia (Fig. 2E, F): Signae long, narrow, parallel,
symmetrical, with short points. Ductus bursae long,
narrow, connected directly to ostium bursae. Ostium
bursae funnel shaped; constricted at bottom, where
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8 L. A. KAMINSKI ET AL.
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thin ductus seminalis emerges. Lamella antivaginalis
lightly sclerotized, flat and slightly notched, with
variable pieces of sclerotized material attached.
Papillae anales rounded.
Variation
This species shows considerable variation in the
extent of the infusion of yellow-orange scaling in
dorsal view, especially in the width and colour of the
post-discal spots, being orange or completely white in
some specimens examined. There is no significant and
consistent geographical variation noted among these
forms between populations.
Immature-stage morphology (Figs 3–8)
The descriptions and measurements of the immature
stage are based on material from both Villa
Giardino (Cordoba) and Volcán (Jujuy), Argentina.
Developmental times were not recorded and should
be variable according to the locality and time of year,
because the first generation that emerges in the spring
should enter larval diapause during the winter.
Egg (Fig. 3): Height 0.58–0.60 mm; diameter 0.76–
0.78 mm (N = 10). Colour whitish cream when laid,
changing to pale green before hatching. General
semispherical shape, with convex upper surface and
flattened bottom surface; exochorion with smooth
surface and covered by hexagonal cells (Fig. 3A).
Several irregular tiny aeropyle openings on the ribs
(Fig. 3B). Micropylar area slightly depressed, with
five micropyles at the centre (Fig. 3C).
First instar (Figs 4A–E, 6C–E, 8D): Head capsule
width 0.29–0.36 mm (N = 10); maximum body length
2.7 mm. Black head; dark grey prothoracic shield
and greyish anal shield; orange-reddish body, with a
longitudinal whitish band dorsally and translucent
setae. Epicranium and frontoclypeus with several
primary setae, pores, and two pairs of PCOs in the
adfrontal areas. Three pairs of thoracic legs of similar
length (Fig. 4A). Body covered by microtrichiae, with
short dendritic setae in the lateral areas (Fig. 4B);
long setae (~500 μm) directed forwards on prothoracic
shield and backwards on anal shield; the remaining
dorsal and subdorsal setae are short and dendritic, and
tiny PCOs (~10 μm) are associated with these groups of
setae (Fig. 4C). Functional TNOs are present in the A8
abdominal segment (Fig. 4D). Proleg with uniordinal
crochets in uniserial lateroseries, interrupted near
centre by conspicuous fleshy pad (Fig. 4E).
Second instar (Fig. 4F–J): Head capsule width
0.47–0.50 mm (N = 5); maximum body length 3.2 mm.
General colour pattern similar to first instar, but
with more intense orange-reddish tones in the body.
Epicranium and frontoclypeus with additional
dendritic setae, pores and PCOs (Fig. 4G). Thoracic
legs of similar length (Fig. 4F). Body covered by
microtrichiae and setae, including scattered dendritic
setae and PCOs dorsally (Fig. 4I), row of mid-sized
setae laterally and posteriorly, and dorsal pairs of
long, clubbed setae on prothorax shield and A1–A7
abdominal segments; these long setae are absent
in meso- and metathoracic segments (Fig. 4F, H).
Functional TNOs are present in the A8 abdominal
segment, delimited by two sclerotized and elevated
plates (Fig. 4J).
Third instar (Fig. 8E): Head capsule width 0.79–
0.80 mm (N = 2); maximum body length 4.4 mm. Head,
prothoracic shield, TNO plates and anal shield black;
body orange-reddish, with longitudinal whitish bands
dorsally. Thoracic legs of similar length; one pair of
vibratory papillae arising on margin of prothoracic
shield. In general, the morphology is similar to that of
Figure 3. Scanning electron micrographs of Aricoris arenarum egg. A, lateral view. B, hexagonal cells of the exochorion
with aeropyles (Ac) in the rib intersections. C, micropylar area (Mp).
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 9
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Figure 4. Scanning electron micrographs of the first (A–E) and second (F–J) instars of Aricoris arenarum. A, lateral view.
B, lateral setae on mesothorax. C, dorsal seta and PCO on mesothorax. D, opening of TNO (arrow). E, proleg of segment A4
in lateroventral view. F, lateral view; note reduce setae on metathorax (arrow). G, head in laterofrontal view. H, dorsal setae
in lateral view; note reduced setae on metathorax (arrow). I, dendritic setae and PCOs on mesothorax. J, opening of TNO
(arrow).
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10 L. A. KAMINSKI ET AL.
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the second instar, including short dorsal setae on the
meso- and metathoracic segments (Fig. 8E), but with
more numerous, longer and thicker setae.
Fourth instar (Fig. 6G): Head capsule width 0.87–
0.90 mm (N = 2); maximum body length 8.7 mm.
Head, prothoracic shield, TNO plates, anal shield
and pinnacles of dorsal setae black with small white
points that correspond to microscopic setae. Body
plum reddish; long setae on prothoracic shield, lateral
and dorsal abdominal areas whitish beige; vibratory
papillae orange. Pairs of long dorsal setae arising on
meso- and metathoracic segments.
Fifth (last) instar (Figs 5A–H, 6F, 8F): Head capsule
width 1.6–1.8 mm (N = 2); maximum body length
21 mm. Head black; prothoracic shield, TNO plates
and anal shield dark grey with small white points that
correspond to microscopic setae. Body pale pink, covered
by small black dots that correspond to microscopic
setae; long setae on prothoracic shield and dorsal
abdominal areas whitish beige; vibratory papillae
orange; lateral setae on body white. Head surface
smooth (Fig. 5A, B), with small spiniform elevations
in cephalodorsal area (Fig. 5E); PCO distribution
scattered, and two types of setae (Fig. 5A, B): filiform
setae directed forwards, ventro-frontally associated
with mouthparts, and short dendritic setae dorso-
frontally. Prothoracic shield with a pair of forward-
directed vibratory papillae at anterior margin (Fig. 5D).
Body covered by microtrichiae and setae, including
dendritic setae and PCOs dorsally (Fig. 5F–H), row of
mid-sized setae laterally and posteriorly, and dorsal
pairs of long, clubbed setae on prothorax shield, meso-
and metathoracic segments and abdominal segments
A1–A7 (Fig. 5A, C). Functional TNOs are present in
abdominal segment A8, flanked by two sclerotized
and elevated plates (Fig. 5A, G). Spiracle (Fig. 5H)
on segment A1 is lateroventral, whereas those on
segments A2–A8 are in a subdorsal position.
Pupa (Figs 5I–L, 6G): Total length 13.8 mm; width
at segment A1 3.2 mm (N = 2). Body brown, with
some beige areas dorsally. Tegument corrugated, with
irregular striations and lacking prominent tubercles
(Figs 5I, 6G); wing case and ventral surface smooth.
Prothorax bears dorsal clusters of short papilliform
setae. Silk girdle crossing abdominal segment A1.
Body with some small dendritic setae, and PCOs
located in clusters on lateral areas close to spiracles
(Fig. 5J, K); these clusters are absent on segments A2
and A7. Scars of TNOs, apparently non-functional, are
present dorsally on A8. The consolidated segments A9
and A10 constitute the ventrally flattened cremaster;
with short crochets in a ventral position (Fig. 5L).
Distribution (Fig. 7)
The known populations present a disjunct distribution
associated with relictual open areas in many parts
congruent with the Peripampasic Orogenic Arc
(Ferretti et al., 2012). The distribution of A. arenarum
is Argentina (from province of Jujuy to La Pampa and
Buenos Aires; Klimaitis et al., 2018), southern Paraguay,
Uruguay and southern Brazil (states of Rio Grande do
Sul and Santa Catarina). A single old specimen from
south-east Brazil (Rio Batalha, state of São Paulo) was
lost in the MNRJ fire in September 2018.
Material examined
Argentina: No locality, one ♂, no. 54/364, MNRJ-
Ent5-14312, ex Coll. E. May, one ♂, no. 54/365 (lost
material) (MNRJ). Buenos Aires: Sierra de la Ventana,
December 1996, one ♀ (CJC), 24 November 2003, one
♀ (CENB), Tandil, December 1957, three ♂, March
1958, one ♂, Collecion Hano (IML), February 1959,
one ♂, MC76790, December 1959, two ♂, MC76793-94,
Collection Biezanko (MCZ). Córdoba: Capilla del Monte
(30°52′S, 64°32′W, 985 m a.s.l.), 28 January 2015, one
♂, one ♀, 26 November 2015, one ♂, L. A. Kaminski leg.
(CLK); Córdoba, 16 November 2005, one ♀ (CJC); La
Cumbre (30°56′S, 64°23′W, 1400 m a.s.l.), 27 January
2015, one ♂, DNA-voucher LAK370, L. A. Kaminski leg.
(CLK). Mina Clavero, 1600 m, 29 January 2003, one
♂, A. Moser leg. (CAM). San Ignacio (30°56′S, 64°31′W,
1053 m a.s.l.), 16 February 2014, two ♂, DNA-voucher
LAK261, LAK262., L. A. Kaminski leg. (CLK). Villa
Carlos Paz, 750 m, 28 January 2003, one ♀, A. Moser
leg. (CAM). Jujuy: Morro de Alizar, 9 January 1977,
two ♂, two ♀, C. Callaghan leg. (CJC). Rio Lozano, 30
September 1976, one ♂, one ♀, C. Callaghan leg. (CJC).
Volcán, Rio del Medio, 1952 m, 21 January 1992, one
♂ (CJC), 28 November 1974, one ♂, one ♀, A. Willink
& Stange leg. (IML). La Pampa: El Carancho (37°26′S,
65°2′W, 320 m a.s.l.), 19 December 2018, two ♂, one
♀, DNA-voucher LAK609, L. A. Kaminski leg. (CLK).
Misiones: Posadas (as ‘Pasadas’ [sic]), December
1922, Joicey Bequest Brits. Mus. 1934-120, NHMUK
013673434. Rio Negro: December 1956, one ♀ (MLP).
Santa Fé: Villa Ana, February 1924, three ♂, one ♀;
October 1924, one ♂; November 1924, one ♂, one ♀;
January 1925, one ♂, one ♀; February 1925, one ♀;
March 1925, one ♂, two ♀; September 1925, three ♂,
five ♀; 10–31 October 1926, one ♂; January 1926, one
♂; February 1926, one ♂, two ♀; March 1926, one ♀,
K. J. Hayward leg. (IML); 1–18 February 1946, one ♀,
K. J. Hayward & A. Willink leg. (IML).
Brazil: Rio Grande do Sul: Caçapava do Sul,
Guaritas (30°49′S, 53°30′W, 250 m a.s.l.), 20 January
2020, one ♂, L. A. Kaminski leg. (CLK). Don Pedrito,
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 11
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Figure 5. Scanning electron micrographs of the last instar (A–H) and pupa (I–L) of Aricoris arenarum. A, head and
thorax in lateral view. B, head in laterofrontal view. C, long dorsal setae on mesothorax. D, vibratory papillae. E, detail of
spiniform elevations (arrow) on cephalodorsal area. F, dendritic setae and PCOs on segment A2. G, opening of TNO (arrow).
H, prothoracic spiracle. I, dorsal view of metathorax. J, cluster of dendritic setae and PCOs above spiracle (sp) on segment
A5. K, detail of dendritic setae and PCOs. L, detail of cremaster crochet.
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12 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
20–21 November 2012, two ♂, two ♀ Romanowski
et al. leg. (DZRS). Encruzilhada do Sul, 400–500 m,
2–3 December 2000, one ♂, A. Moser leg. (CAM).
Estação Ecológica do Taim, 13 January 1999, two ♂;
4–7 March 2013, one ♀, A. Moser leg. (CAM); 7 March
2013, two ♀, CLDZ 9252–9253; 25–26 November
2013, five ♂, three ♀, CLDZ 9247–9251, 9254–9256,
H. P. Romanowski et al. leg. (DZRS); 7 March 2013,
one ♂, DNA-voucher LAK228, V. Pedrotti & A. Moser
leg. (CAM). Jaguari, 16 January 2001, one ♂,
Figure 6. Life cycle of Aricoris arenarum tended by ‘black morphs’ of Camponotus punctulatus ants on Geoffroea decorticans
(Fabaceae), showing both free-living and social parasitic phases. A, female at post-alighting phase. B, eggs close to ant-
tended treehoppers (dashed ellipse). C, eggs (white arrows) and first instar caterpillars (black arrows) close to scale insets,
both tended by ant workers. D, first instar caterpillar (black arrow) close to ant-tended treehoppers. E, sequence of worker
drinking honeydew from treehopper (top panel, white arrow) and first instar requesting trophallaxis from ant (bottom
panel, white arrow); note the typical larval posture and long prothoracic setae. F, last instar caterpillar tended by ants
inside brood chamber. G, penultimate instar (black arrow indicates the everted larval TNO) and pupa inside the ant nest
(white arrow). Scale bars: 5 mm in A, B, C, D, F, G; 2 mm in E.
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 13
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A. Moser leg. (CAM). Jari, 23 November 2011, one
♂, CLDZ-8021 (DZRS). Pelotas, 30 November 1956,
one ♂, C. Biezanko leg. DZ 38.500; 25 November
1957, one ♂, J. L. Mantovani leg., DZ 38.350 (DZUP).
Pinhal, April 1971, one ♂, C. A. Trois leg. (DZRS).
Santa Maria, 2–8 November 1972, three ♀, DZ
38.680, DZ 38.300, DZ 38.630 (DZUP). São Leopoldo,
8 January 1994, four ♂, one ♀; 15 January 1994,
one ♂, A. Moser leg. (CAM). Vacaria, Bela Vista,
one ♂ (DZUP). Viamão, Parque Estadual de Itapuã
(30°23′S, 51°17′W, 5 m a.s.l.), 20 January 2002, one
♀; February 2002, one ♂, E. C. Teixeira leg. (DZRS).
Torres, Praia Paraiso, 13–17 March 2012, one ♂, one
♀, A. Moser leg. (CAM). Tupanciretã, 16 March 2012,
one ♀, CLDZ 8022, B. O. Azambuja leg. (DZRS). São
Paulo: Rio Batalha, one ♀, no. 54/368 (lost material)
(MNRJ). Santa Catarina: Curitibanos, 7 March 1983,
one ♂, one ♀ H. Miers leg. OM67315, OM67637 (OM).
Paraguay: No locality, one ♂, Crowley bequest 1901-
18 (NHMUK). Guairá: Villarica, 20 March 1930, three
♂, two ♀ (MLP); 20 February 1950, one ♂, one ♀,
Collecion Breyer (IML). Paraguari: Mbopicua (26°20′S,
57°8′W, 110 m a.s.l.), 9 March 2014, one ♂, DNA-
voucher LAK133, L. A. Kaminski leg. (MNHNPA),
Sapucai, 10 December 1902, one ♀; 30 March 1903,
one ♂; 1 November 1903, one ♂; 17 November 1904,
one ♂; 23 December 1904, one ♂; 19 November 1904,
Figure 7. Map of South America (top left) and detail of topographic map of Río de la Plata basin (red rectangle) showing the
geographical distribution of Aricoris arenarum (red circles), type locality in Uruguay (yellow star) and overview of studied
vegetation habitats (black circles). A, mountain Chaco in Volcán, Jujuy, Argentina. B, mountain Chaco in Capilla del Monte,
Córdoba, Argentina. C, dry Espinal in El Carancho, La Pampa, Argentina. D, Pampean grassland in Castillos, Uruguay. E,
coastal sand grasslands in Parque Estadual de Itapuã, Viamão, Rio Grande do Sul (RS), Brazil. F, grassland–Atlantic forest
mosaic in Vacaria, RS, Brazil. G, natural grasslands in Mbopicua, Paraguari, Paraguay. Dashed white line delimits the
Peripampasic Orogenic Arc (modified from Ferretti et al., 2012), and black dashed line indicates the life cycle study sites (A,
B, D, respectively).
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14 L. A. KAMINSKI ET AL.
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one ♂, W. Foster leg., Rothschild Bequest B. M. 1939-1
(NHMUK).
Uruguay: Canelones: Castillos (33°49′S, 57°40′W, 90 m
a.s.l.), 23 January 2020, one ♂, three ♀, L. A. Kaminski
leg. (CLK). Las Piedras, 12 September 1976, one ♀,
A. Carmenes leg. (FCE-LP). Lavalleja: Minas, Cerro
Arequita (34°17′S, 55°16′W, 155 m a.s.l.), 23 January
2020, one ♂, L. A. Kaminski leg. (CLK). Maldonado: La
Barra, 29 November 1936, one ♂, one ♀, H. Schneider
leg. (ZFB). Montevideo: Montevideo, 13 November
1926, one ♀, Col. De S. Dobree, (NHMUK). Treinta y
Tres: Santa Clara, 17 February 1960, one ♂, MC76792,
L. Zolessi leg., Collection Biezanko (MCZ).
Behaviour and natural history
Populations of A. arenarum are found located at
particular sites. Females have a slow and passive
flight, a feature first noted by Schneider (1937).
During the late afternoon (13.00–18.00 h), males
can be observed lekking in small territories in the
same places. The physiognomy of the vegetation of
these sites ranges from mountain Chaco habitats
(Fig. 7A, B), with sparse shrubs and an abundance of
‘espinillo’ Vachellia caven (Molina) Seigler & Ebinger
and ‘chañar’ Geoffroea decorticans (Gillies ex Hook. &
Arn.) Burkart (Fabaceae), to dry Espinal (Fig. 7C) and
Pampean grasslands, from coastal sand dunes (type
locality) to highlands in the Atlantic Forest domain
(Fig. 7D–G) (for details of vegetation types see Cabido
et al., 2018; Oyarzabal et al., 2018).
These sites are always occupied by large polydomic
colonies of ‘black morphs’ of C. punctulatus. This
dominant ant nest in the ground is active both during
the day and at night and monopolizes the liquid food
sources on plants, such as extrafloral nectaries and
honeydew-producing hemipterans. For taxonomic
details of this polytopic ant species and discussion
about red and black morphs see Kusnezov (1952).
The females of A. arenarum spend the hottest
hours of the day in searching for ant trails and laying
eggs on the vegetation (Figs 6A, B, 8C), always near
hemipteran aggregations tended by C. punctulatus
(Fig. 6C–E). We found caterpillars associated
with four scale insect (Coccoidea) morphotypes
and one treehopper (Membracidae) species. Some
plants could contain dozens of eggs, many of which
proved infertile. Oviposition was observed several
times (N = 12 in Argentina, N = 2 in Uruguay).
Substrates for oviposition include different host
plant families, primarily grass species (Poaceae) in
Pampean grasslands and scrub species in mountain
chaco, such as Geoffroea decorticans and Galactia
marginalis Benth. (Fabaceae), the invasive Pastinaca
sativa L. (Apiaceae), Schinus fasciculata (Griseb.)
I.M.Johnst. (Anacardiaceae), Baccharis ulicina Hook.
& Arn. (Asteraceae) and Gnaphalium sp. (Asteraceae).
Although females can lay their eggs remarkably close
to ant–hemipteran associations, the ants are often
aggressive and try to prevent oviposition.
First and second instar larvae live together with
ant–hemipteran associations (Fig. 6C–E); while the
ants tend the hemipterans, the caterpillars await the
release of honeydew, stealing the drops before the
ants can feed. In the laboratory, a first instar larva
was observed cannibalizing a conspecific egg. Plants
infested by scale insects and treehoppers that are
heavily tended by ants can harbour many caterpillars
(15–20). These caterpillars can also request honeydew
from hemipterans through rapid head movements; this
behaviour was observed when the ants were absent in
the field and laboratory. Caterpillars can also receive
food resource via trophallaxis directly from ants; for
this, they raise the anterior portion of the body and
touch the ant mouthparts with their long, forward-
directed prothoracic setae (Fig. 6E).
From the third instar on, the caterpillars change
the free-living behaviour on plants to a social parasitic
lifestyle within the ant nest. The details of how this
transition takes place are still unknown. We never
found mature larvae (from the third instar on) on
the plants, only first and second instars. During the
excavation of the base of a plant previously occupied
by larvae, we found a third instar caterpillar buried
~20 cm below the ground, apparently following the ant
trails. In Córdoba, we excavated several ant nests in
search of caterpillars, but we did not find any. In Jujuy,
mature caterpillars were found inside brood chambers
of C. punctulatus [cited as Camponotus distinguendus
(Spinola, 1851) by DeVries et al., 1994; DeVries, 1997]
immediately underneath the stones in a rocky field;
probably, they were warming up on a cold day together
with the ant brood.
In the laboratory, caterpillars from both Córdoba
(first to third instars) and Jujuy (last instar)
populations were offered plant material (grass and/
or chañar) with honeydew-producing hemipterans,
and both living and macerated ant brood, but the
caterpillars did not feed on them. Third instar larvae
placed inside the experimental ant nest completed
their development without the availability of food
plant items and/or honeydew-producing hemipterans.
During the parasitic phase, the caterpillars remained
in the ant brood chambers and received trophallaxis
from the worker ants (Figs 6F, G, 8F). There were
no agonistic interactions between larvae and ants.
Workers occasionally antennated the caterpillars,
especially on segment 8A near the TNOs. In response,
the larvae everted the TNOs, but without providing
visible secretions. Pupation took place inside the ant
nests (Fig. 6G).
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DISCUSSION
Ant colonies are homeostatic fortresses with complex
communication and recognition systems (Hughes
et al., 2008). Many organisms can circumvent these
security systems and live as social symbionts within
the ant nest (Hölldobler & Wilson, 1990). Multiple
transitions from pre-adapted free-living ancestors
to social parasitism have been documented in
myrmecophilous beetles, illustrating the predictability
of this evolutionary process (Maruyama & Parker,
2017). In butterflies, social parasitism appeared a few
times in Lycaenidae through different evolutionary
routes (Cottrell, 1984; Pierce, 1995; Osborn & Jaffé,
1997; Fiedler, 1998). Riodinidae, the sister family that
diverged ~90 Mya (Espeland et al., 2018; Fig. 8A),
shares pre-adaptive traits (e.g. PCOs) and developed
ant-organs analogous to those of Lycaenidae that also
enable myrmecophily (DeVries, 1991b). The discovery
of social parasitism in Riodinidae offers the opportunity
for a deeper analysis of the different evolutionary
routes that lead to social parasitism in butterflies. In a
comparative framework, Fiedler (1998) proposed three
types of lycaenid–ant parasitism: (1) the Miletinae
type, derived from a hemipteran-predator ancestor;
(2) the Aphnaeini type, derive from an ancestor with
obligate myrmecophily; and (3) the Maculinea type,
derived from a facultative myrmecophilous ancestor.
In addition, Fiedler (1998) pointed out that social
parasitism occurs predominantly in highly seasonal
habitats and suggested that this phenomenon started
with caterpillars seeking shelter in ant nests.
The case of A. arenarum fits the Aphnaeini type,
because most known Aricoris species are phytophagous
and establish obligate trophobiotic interactions with
their tending ants (Kaminski & Carvalho-Filho, 2012;
Volkmann & Kaminski, 2015). Thus, the evolution of
social parasitism within Aricoris must be much younger
than the estimated age for the split between Ariconias
and Aricoris (~11 Mya; Seraphim et al., 2018; Chazot
et al., 2019). These butterflies have diversified widely
in the open and/or dry seasonal areas of South America
(Caatinga, Cerrado, Chaco and Pampa), and the use
of underground shelter during the day is a behaviour
likely to be associated with their success in extreme
environments. Thus, in addition to escaping daytime
predation, the caterpillars can escape from the typical
high temperatures of these environments. During the
cold or dry winter months, the Aricoris caterpillars
usually go into diapause within these underground
shelters (DeVries, 1997; Volkmann & Kaminski,
2015). Both behaviours agree with the idea of the
importance of abiotic factors (seasonality) and use of
ant shelters for the evolution of social parasitism. In
contrast, the key to the evolution of social parasitism
in A. arenarum seems to be the kleptoparasitic
exploitation of ant–hemipteran mutualistic systems
through tactile mimicry.
The detailed comparison with N. fusca, a n
Asian Lycaenidae with a remarkably similar life
cycle, supports this hypothesis. Both species occur
in a subtropical to temperate climate and are
associated with a dominant Camponotus species. The
A. arenarum and N. fusca females oviposit only in the
presence of ant–hemipteran associations. Throughout
the ontogeny, the morphology of the caterpillars is
extremely similar, generally through convergent
evolution, although some traits seem to represent
cases of parallelism (Fig. 8; Table 1). In the first instar,
the long, forward-directed setae are present on the
thorax and are used to request hemipteran honeydew
(Fig. 8D, H). The comparative analysis of chaetotaxy
indicates parallelism for the setae on the prothorax,
with homologous setae performing the same function,
whereas the dorsal mesothoracic setae are elongated
only in Niphanda, indicating convergence. In the
second instar, long setae occur dorsally along the body,
except for the metathorax, which presents short setae
(Fig. 8E, I). This reduction of the metathoracic setae
facilitates the movement of the anterior portion of the
body, which is essential for reaching the mouth of the
ant during trophallaxis. In ants, trophallaxis is induced
by a simple tactile communication mechanism (the
touch of the labium by antennas or legs), and different
lineages of kleptoparasites use different structures to
request ant regurgitations through tactile mimicry
(Hölldobler & Wilson, 1990). In addition to the food
resource, it has recently been shown that trophallaxis
might also transfer social information (Hayashi et al.,
2017). Thus, ant regurgitations might contain the
access key to the ant nest, a hypothesis that needs to
be tested.
In N. fusca, adoption is mediated by tentacle organs
(TOs) in the third instar (Nagayama, 1950; Hojo
et al., 2014), but we still do not know whether active
adoption by tending ants occurs in A. arenarum. The
TNOs of A. arenarum have lost the main riodinid
function of producing nutritional rewards and appear
to play a direct role in chemical communication with
ants. These organs are homologous in position with
Lycaenidae TOs, which are also used exclusively for
chemical communication (Henning, 1983; Axén et al.,
1996; but see Gnatzy et al., 2017). At the same time,
the anterior tentacle organs (ATOs), which are present
in Aricoris and related genera in Lemoniadina, with
a functional role in chemical communication (Ross,
1966; DeVries, 1988), have been lost in A. arenarum.
Thus, a functional reorganization of these ant-organs,
unique among the Riodinidae, has resulted in a body
plan and functioning remarkably similar to that of
Lycaenidae, i.e. tentacle organs only in the eighth
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16 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
Figure 8. Comparative phylogenetic position, geographical distribution and life cycles of two ‘cuckoo’ butterflies:
‘Hormiguera Chopí’ Aricoris arenarum (orange lines) and ‘Kuro-shijimi’ Niphanda fusca (blue lines), respectively. A,
phylogeny of Riodinidae and Lycaenidae based on the study by Espeland et al. (2018), showing estimated dated origins
of myrmecophily (black dots), social parasitic lineages (yellow dots) according to Fiedler (2012) and an unconfirmed case
(yellow dot with question mark). Orange, A. arenarum; blue, N. fusca. B, world map indicating continental records of social
parasitism in butterflies. C–F, A. arenarum life cycle sequence, illustrating: C, female oviposition close to ant–hemipteran
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THE FIRST RIODINID ‘CUCKOO’ BUTTERFLY 17
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
abdominal segment and apparently used for chemical
communication. The functional plasticity of ant-organs
seems to be a recurring phenomenon in riodinids
(Kaminski, 2008; Nielsen & Kaminski, 2018). We do not
yet know the role of circular hydrocarbons in chemical
mimicry in A. arenarum, but this is a key process in
N. fusca and other social parasitic caterpillars (Akino
et al., 1999; Hojo et al., 2009). Although the acoustic
context has not yet been explored in Niphanda and
Aricoris, all species of the latter genus that have been
studied present structures potentially used for acoustic
communication (vibratory papillae; Fig. 5D–E), as
observed in other social parasitic systems (DeVries
et al., 1993; Barbero et al., 2009).
Although parasitic caterpillars show spectacular
cases of convergence, they can also be markedly
different depending on the ecological context. Some
parasitic caterpillars are defended by a thick cuticle
and modified setae that prevent ant attacks and allow
them to enter the ant nests forcefully (e.g. Dupont et al.,
2016), in which case the caterpillar–ant interaction is
basically antagonistic (Miletinae type). The Maculinea
type involves an herbivorous phase and neotenic-looking
caterpillars that use multimodal sensorial mimicry to live
in ant nests (Casacci et al., 2019). The Aphnaeini type can
include different multifaceted strategies and, possibly,
this type should be split into several biological groups
(see discussion by Cottrell, 1984; Osborn & Jaffé, 1997;
Boyle et al., 2015). Overall, this categorization reflects
different basic eco-evolutionary pathways that resulted
in a suite of ecomorphological homoplasies shared
within the members of each type. The extraordinary
similarity between A. arenarum and N. fusca shows that
the exploitation of symbiotic systems involving plants,
hemipterans and ants in a similar ecological context
can result in similar morphological and behavioural
solutions, even in deeply diverged lineages, illustrating
the importance of convergent multispecies interactions
in evolution (Bittleston et al., 2016).
concluding reMarks
The life cycle of A. arenarum is described, which
represents the first ‘cuckoo’ caterpillar in Riodinidae.
association (dashed ellipse); D, first instar feeding on hemipteran honeydew (dashed ellipse); E, third instar with reduced
setae on metathorax (yellow arrow) feeding on ant regurgitation (dashed ellipse); F, last instar inside ant nest. G–J, N. fusca
life cycle sequence, depicting: G, sequence of female oviposition (dashed ellipse); H, first instar feeding on hemipteran
honeydew (dashed ellipse); I, third instar with reduced setae on metathorax (yellow arrow) feeding on ant regurgitation
(dashed ellipse); J, last instar inside ant nest.
Table 1. Homoplastic ecomorphological traits shared between Aricoris arenarum (Riodinidae) and Niphanda fusca
(Lycaenidae) (for details, see Fig. 8 and Discussion)
Ecomorphological trait Potential type of
homoplasy
Hypothetical adaptive significance
Ant–hemipteran-dependent oviposition Convergence Increases the likelihood of
interaction
Loss of plant specificity and oviposition on
Poaceae
Convergence Exploitation of new ant–plant–
hemipteran systems
Feed on liquids (hemipteran honeydew and
ant regurgitations)
Convergence Reduction of symbiotic cost by not
feeding directly on plant tissue,
hemipterans or ants
Social parasitism Convergence Stable and enemy-free environment
(ant nest) during cold months and
nutritional benefits
Pinkish last instar caterpillars Convergence Lack of plant pigments and/or no
selection for visual crypsis
Long thoracic setae directed forwards Parallelism and
convergence
Tactile communication with
hemipterans and ants
Reduction of dorsal setae on metathorax Parallelism Improved mobility of the anterior
portion, facilitating ant
trophallaxis
Tentacle organs on eighth abdominal segment Convergence and
parallelism
Chemical communication with
tending ants
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18 L. A. KAMINSKI ET AL.
© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–20
Ecomorphological traits are compared with those of
parasitic Lycaenidae, in particular with those of the
Asian N. fusca. Despite divergence ~90 Mya, multiple
traits show remarkable homoplasy between these
two species, either through convergence or through
parallelism. This discovery provides new insights into
the evolution of social parasitism in butterflies and
shows that ecological determinants (e.g. the parasitic
strategy and host ant system) are more important than
phylogenetic proximity in shaping the morphological
and behavioural traits of social parasites. The tortuous
taxonomic history of A. arenarum, spending > 80 years
in limbo, exemplifies the current state of knowledge
about the diversity of this family of butterflies. There
are shortfalls at all levels, from alpha taxonomy, which
generates taxonomic impediments, to basic natural
history information (DeVries, 1997). Although much
recent effort has been made to address the taxonomy
and evolution of these butterflies (e.g. Dolibaina et al.,
2013; Espeland et al., 2015, 2018; Hall, 2018; Seraphim
et al., 2018), many gaps still exist, and cryptic diversity
is poorly explored. New findings of caterpillars within
ant nests, such as Alesa rothschildi (Seitz) in the
Amazon canopy (see Gallard, 2017) and unpublished
anecdotal observations by the authors suggest that
social parasitism in riodinids might have arisen
independently in all Nymphidiini subtribes and,
possibly, also in Eurybiini (Fig. 8A). As exemplified by
the present study, each discovery in Riodinidae might
reveal new strategies and possibilities of convergence
with Lycaenidae. This diversity is severely threatened
by anthropic activity, and the description of vanishing
yet-unknown life cycles and evolutionary pathways is
urgent, even more so for their protection.
ACKNOWLEDGEMENTS
We are grateful to Adriana Chalup, Alexandre Soares,
Alfred Moser, Blanca Huertas, Bolívar R. Garcete
Barrett, Fernando Navarro (in memorium), Eurides
Furtado, Ezequiel Núñez Bustos, Gabriela Bentancur-
Viglione, Helena P. Romanowski, John A. Kochalka,
Marcelo Duarte, Mirna M. Casagrande, Olaf H. H.
Mielke and Sérgio Rios for allowing us to examine the
specimens and for the loan of material for dissection.
Special thanks to Gerardo Lamas for his fundamental
help in locating the Schneider specimens at the ZfB,
Saarland Museum and for helpful comments on the
taxonomic issues, and to Dr Andreas Werno, curator
at the ZfB, for providing photographs and information
on the specimens. Thanks to Gerard Talavera, John
A. Kochalka, Julio Guevara, Luiza Magaldi, Luan
D. Lima, Matias Köhler and Sérgio Rios for help
with the fieldwork. Thanks to Alan Heath, Masaya
Yago and David J. Lohman for help with African and
Japanese literature. Thanks to José R. A. Lemes,
Keith R. Willmott, Konrad Fiedler, and an anonymous
reviewer for critical reading of the manuscript.
Financial support for this research was provided
by National Geographic Society (WW-224R-17) and
a Programa Nacional de Pos-Doutorado (PNPD)-
Coordenação de Aperfeicoamento de Pessoal de
Nivel Superior (CAPES) fellowship to L.A.K., and
by the Spanish Ministerio de Ciencia, Innovación
y Universidades (PRX19/00067 and PID2019-
107078GB-I00 / AEI / 10.13039/501100011033) to R.V.
This paper is dedicated to Ivone Erichsen (1937–2019)
and Beatriz D. Ponce (1933–2016) for fundamental
symbiotic support to L.A.K. and L.V., respectively.
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