Aricoris arenarum ( Schneider, 1937 )

Kaminski, Lucas A., Volkmann, Luis, Callaghan, Curtis J., Devries, Philip J. & Vila, Roger, 2020, The first known riodinid ‘ cuckoo’ butterfly reveals deep-time convergence and parallelism in ant social parasites, Zoological Journal of the Linnean Society 193, pp. 860-879 : 863-873

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 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 M 3 is displaced distally, aligned to that in cell M 2. Internally, A. arenarum male genitalia ( Fig. 2B–D ) 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).

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; R 1 and R 2 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 M 1, then curved abruptly to anal angle; the distal margin slightly indented between Cu 2 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 Cu 2; distad an irregular post-discal band of white spots from cells R 2 to 2A, edged basad in black and variably infused with orange scaling; the second middle spot offset distally, the next two in cells M 2 and M 3 together, those in cells Cu 2 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 M 2 and M 3 offset distad; limbal area orange containing a submarginal row of black spots, one in each cell except Cu 2 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 Cu 2 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 M 2 to Cu 2; 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 yelloworange 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 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 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 dorsofrontally. Prothoracic shield with a pair of forwarddirected 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: R i o G r a n d e d o S u l: C a ç a p av a d o S u l, Guaritas (30°49′S, 53°30′W, 250 m a.s.l.), 20 January 2020, one ♂, L. A. Kaminski leg. (CLK) . Don Pedrito, 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 ♂, 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 ♂, DNAvoucher 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, 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, forwarddirected 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 ).

Figures

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.

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.

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).

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).

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.

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 anttended 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.

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).

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 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.