Formicidae Latreille, 1809

Boudinot, Brendon E., 2015, Contributions to the knowledge of Formicidae (Hymenoptera, Aculeata): a new diagnosis of the family, the first global male-based key to subfamilies, and a treatment of early branching lineages, European Journal of Taxonomy 120, pp. 1-62 : 12-17

Family Formicidae Latreille, 1809

Diagnosis

Aculeate Hymenoptera with the following apomorphies:

1. Eusocial, wingless worker caste present, colonies perennial (note 1).

2. Sexuals with synchronous nuptial flights (note 2)

3. Head capsule prognathous (worker, gyne) (note 1).

4. Infrabuccal sac present between labium and hypopharynx (note 1).

5. Antenna geniculate between long scape and funiculus (worker, gyne) (notes 1, 3).

6. Disticoxal foramen directed laterally and completely enclosing protrochanteral base, including protrochanteral condyles, such that all disticoxal membrane concealed (all castes, Fig. 3C) (note 4).

7. All meso- and metacoxal cavities small, circular, monocondylic, ventrally-directed, and disticoxae strongly produced laterally (all adult castes, Fig. 3C) (note 5).

8. Metapleural gland present (adult castes, but see note 6).

9. Propodeal spiracle located on lateral propodeal face distant from the anterodorsal propodeal corner, often near propodeum midlength (all adult castes) (note 7).

10. Wings of alate gyne deciduous, being shed after copulation (note 1).

11. Forewing 3rs-m and 2m-cu absent (note 1).

12. Hindwing C not extending along anterior margin, even spectrally (note 8).

13. Hindwing basal/radial cell not produced distally (alate castes) (note 9).

14. Metasoma petiolate (abdominal segment II differentiated from segment II,I which is strongly constricted between the pre- and postsclerites) (all castes), extremely rarely (~ 1 species) abdominal segment III not constricted between pre- and postsclerites (notes 1 and 10).

Additional, non-synapomorphic characters of value for diagnosis and identification include: Antenna with 4–12 antennomeres (female) or 5–13 antennomeres (male) (note 11). Bulbus neck (= radicle) and scape with common axis. Epicnemium extremely reduced, not visible in situ (note 12). Abdominal segment II with sternum and tergum equally sclerotized. Pterostigma present or absent (note 13). Wing venation variable, may be extremely reduced, with at minimum no closed cells (note 14). Jugal lobe present or absent; abdominal sternum IX may be complex and modified apically (including prongs, teeth, and lobes).

Notes

1. Noted as apomorphic by Bolton (2003).

2. Bolton (2003) indicated that “sexuals with mass nuptial flight” was an apomorphy of the Formicidae . Although mass flights do occur in several lineages of ants, it is not clear if the ancestral condition for the Formicidae is to release large quantities of sexuals. The wording has been specifically rephrased here to account for this uncertainty.

3. Males of many species have derived geniculate antennae with elongate scapes, including numerous Myrmicinae , most Formicinae , and Tapinoma (Dolichoderinae) . Most males, including poneroids and numerous formicoids, however, have antennae which are not geniculate and have very short scapes.

4. The procoxa of Formicidae is characteristically modified. The trochanteral foramen (situated apically on the procoxa) is directed laterally and entirely enclosed, revealing no membrane in undamaged specimens ( Fig. 3C, left column, top row). Medially, the foramen is closed by an unfused seam of the anterior and posterior apical coxal lobes, which completely surround the anterior trochanteral process. The axis of coxal-trochanteral articulation, rather than being lateromedial as in Symphyta ( Fig. 3A), or rotated obliquely as in many Aculeata ( Fig. 3B), is almost entirely anteroposterior. Leg adduction and abduction occurs along this anteroposterior axis in more-or-less one plane of motion, with the trochanter rotating within the closed disticoxal foramen. The coxae and their articulations with the mesosoma and trochanters are poorly studied and show promise for valuable systematic characters. Previous work on hymenopteran coxae include Johnson (1988), which solely focused on the basicoxite and its musculature, Michener (1981), which focused on the meso- and metacoxae of the Apoidea, and Vilhelmsen et al. (2010), which operationalized several coxal characters. This character is unique to the Formicidae .

5. The meso- and metacoxal foramina are monocondylic, bearing only the medial coxal articular processes and lacking the lateral coxal articular processes of the meso- and metapleurae. Lateral condyles are lacking in the examined species of Chyphotinae , Bradynobaenidae s. str., Mutillidae , and Myrmosidae .

6. The metapleural gland, so distinctive of the female castes, is variably developed in males and has been lost in various taxa.

7. The “high and far forward” placement of the propodeal spiracle remarked upon by Bolton (2003) as a plesiomorphy for the Formicidae is actually an apomorphy for the family. In non-formicid Aculeata (including Apoidea, Scoliidae , and Bradynobaenidae s. str.) the propodeal spiracle is usually situated at the extreme anterodorsal corner of the propodeum, usually within a propodeal spiracle length from the metanotum, and often on the dorsal propodeal face. Some Pompilidae and Tiphiidae (Tiphiinae) have the spiracle situated more posteriorly. Although the propodeal spiracle of † Sphecomyrma freyi is situated high—but laterally—and rather anteriorly ( Wilson et al. 1967), it is clearly not at the extreme of other Aculeates. Other † Sphecomyrma species have more posteriorly situated spiracles which are clearly situated laterally ( Wilson 1985; Engel & Grimaldi 2005). The potential male of † Sphecomyrma identified by Grimaldi et al. (1997) has a low spiracle situated at about segment midlength.

8. Reduction of the hindwing costal vein occurs sporadically in other aculeate families.

9. The basal/radial cell has been convergently reduced or lost in several ant subfamilies, and has been lost in Mutillidae , Myrmosidae , Bradynobaenidae s. str., and Chyphotidae . The generality of this trait in these families was not evaluated.

10. The male of an unidentified Protanilla (Leptanillinae) from Thailand has secondarily lost petiolation, where the third abdominal segment is no longer constricted between the pre- and postsclerites ( Fig. 10A ). These males are still recognizable as ants by the closed apical procoxal foramen, ventrallydirected meso- and metacoxal cavities, and low and lateral propodeal spiracle. Other Protanilla species (even in sympatry) retain the constriction, while yet others have petiolation of the third abdominal segment ( Fig. 10B ). Some males of the Dolichoderinae (e.g., Azteca ) and other unidentified males of the Leptanillinae have very reduced petioles, but these are still distinctly differentiated from the third abdominal segment and are slightly posteriorly constricted.

11. Antennomere count for males usually 13, less often 8–12 (count of 8 observed in Acropyga and Stenamma ; counts of 10+ more common). Antennomere counts may be extremely reduced in inquilines, for example in Pheidole acutidens , which occasionally have an antennomere count of 5, although this is variable infraspecifically, and indeed may vary between the left and right antennae.

12. Brothers (1975) contends that the form of the formicid epicnemium is unique, being highly reduced, fused to and extending over the height of the mesepisternum, and obscured by the pronotum. This putative homology was not evaluated in the present work.

13. The pterostigma is lost in most Leptanillinae , some myrmicine genera, and some species of Leptomyrmex (Dolichoderinae) .

14. No closed cells are observed in some males of Leptanillinae and Myrmicinae .

Remarks

The Formicidae is an unequivocally monophyletic group, previously defined by Bolton (1994, 2003) as eusocial, sexually dimorphic aculeate Hymenoptera bearing metapleural glands and geniculate antennae, among other characters. Several previously unreported synapomorphies exist for the family, including a suite of adaptations for terrestrial locomotion (characters 6 and 7). The “low and lateral” propodeal spiracle placement may also be an adaptation for terrestrial locomotion, as it may reduce the distance oxygen would need to diffuse to leg locomotor muscles. While this does not clarify whether the ancestral ant was hypogaeic or epigaeic, it does indicate that terrestrial locomotion was a crucial transition for the Formicidae , as these apomorphies are present in all adult castes of the family. Previous diagnoses of the family ( Brothers 1975; Gauld & Bolton 1988; Goulet & Huber 1993) were significantly improved by Bolton (1994, 2003). Characters indicated in the family diagnosis by Bolton (2003) and above will be valuable to evaluate for critical fossil taxa such as † Armania Dlussky and other fossils assigned to the † Armaniidae whose relationship to the Formicidae is uncertain (see Dlussky 1975: † Archaeopone , † Dolichomyrma , † Poneropterus , † Pseudarmania ; Dlussky 1983: † Armaniella ; Dlussky 1999: † Khetania ; Dlussky et al. 2004: † Orapia ; also see discussion in LaPolla et al. 2013).

Key to global subfamilies, based on extant males

Notes: It may be expected that some taxa will fail this key, as males of at least 70 genera are undescribed and/or uncollected (see subfamily diagnoses for specific genera). This key treats alate males only, because ergatoid males are identifiable similarly to the workers. Ergatoid males generally bear shorter scapes and more antennomeres than the female, and are known for about a dozen genera.

1 Apicolateral corners of abdominal sternum IX pronged or toothed (even if minutely) ( Fig. 4 A–B)… 2

– Apicolateral corners of abdominal sternum IX lobed or rounded ( Fig. 4C )…………………… 3

2 Petiole hatchet-shaped in profile view, with distinct peduncle, and node with distinct anterodorsal angle in profile view ( Fig. 4D ). Clypeus well-developed, with conspicuous convex median disc. Pretarsal claws cleft. Pygostyles present. Neotropical……………… Paraponerinae (Paraponera)

– Petiole nodiform, fusiform, subrectangular, or cylindrical in profile view, with or without a distinct peduncle, and node without anterodorsal angle in profile view ( Fig. 4E ). Clypeus poorly developed, more-or-less linear, without conspicuous convex median disc. Pretarsal claws not cleft; claws edentate or toothed. Pygostyles absent.Global……… Dorylinae (part, excluding Leptanilloides genus group)

3 Wing venation reduced to extremely reduced, with at most only Sc+R+Rs, Rsf1, Mf1, M+Cu, and 1r-rs+Rsf4–6 tubular, at most only three closed cells present (costal, basal, subbasal) ( Fig. 4F ) and propodeal lobes very inconspicuous or absent ( Fig. 4G ). Old World………………… Leptanillinae

- Wing venation more complete, often more than three closed cells present or propodeal lobes conspicuous and present ( Fig. 4H ). Global………………………………………………………… 4

4 Abdominal segment III strongly reduced and differentiated from abdominal segment IV ( Fig. 5A, B) and antennal toruli separated from anterior clypeal margin by at least one antennal socket diameter and terminal abdominal tergum never produced as spine………………………………… 5

– Abdominal segment III not reduced relative to abdominal segment IV or somewhat reduced, but not differentiated from abdominal segment IV ( Fig. 5C) or antennal toruli separated from anterior clypeal margin by less than one antennal socket diameter or terminal abdominal tergum posteriorly produced as spine……………………………………………………………………… 8

5 Metatibia with 2 ventroapical spurs (anterior spur may be reduced in size)……………………… 6 – Metatibia with at most 1 ventroapical spur………………………………………………………… 7

6 Jugal lobe present. Frontal carinae usually robust and conspicuous ( Fig. 5D). Cuticle very thick and usually coarsely sculptured. Australia ………………… Myrmeciinae , part( Myrmeciini : Myrmecia )

– Jugal lobe absent. Frontal carinae fine, inconspicuous, or absent ( Fig. 5E). Cuticle thin and usually finely to not sculptured. New World; African, Asian, Australian………………… Pseudomyrmecinae

7 Abdominal tergum IV strongly and evenly convex in profile view and much longer than abdominal sternum IV ( Fig. 5F, black lines). Helcium supraaxial: Anteroposterior axis of helcium situated well above anteroposterior axis of abdominal segment III postsclerites, such that poststernite with very dorsoventrally tall anterior face relative to anterior face of posttergite ( Fig. 5F, dark green lines along anterior faces of abdominal segment III). Spiracle of abdominal tergum IV located in extreme anteroventral corner(within at least five spiracular diameters)……… Agroecomyrmecinae (Tatuidris)

– Abdominal tergum IV weakly or unevenly convex in profile view and about as long as abdominal sternum IV ( Fig. 5G, black lines). Helcium axial: Anteroposterior axis of helcium situated at about midheight of abdominal segment III postsclerites, such that anterior faces of postsclerites roughly equivalent, or anterior face of posttergite somewhat longer than that of poststernite ( Fig. 5G, green lines). Spiracle of abdominal tergum IV located distant from anteroventral corner (distant by at least ten spiracular diameters)…………………… Myrmicinae

8 Abdominal segment IV with cinctus (constriction) between the pre- and postsclerite ( Fig. 5H) or jugal lobe present or oblique mesopleural sulcus absent or indistinct……………………………… 9

– Abdominal segment IV without a cinctus ( Fig. 5I) and jugal lobe absent and oblique mesopleural sulcus always present……………………………………………………………… 19

9 Antennal toruli situated anteriorly, abutting, very nearly abutting, or overhanging anterior clypeal margin; toruli less than one antennal socket diameter from anterior clypeal margin in frontal view ( Fig. 6A ) …………………………………………………………………………………………… 10

– Antennal toruli situated posteriorly; toruli distant from anterior clypeal margin by at least one antennal socket diameter in full-face view ( Fig. 6B )………………………………………… 12

10 Abdominal segment IV with distinct cinctus between pre- and postsclerites. Oblique mesopleural sulcus present ( Fig. 6D ) or absent………………………………………………… 11

– Abdominal segment IV without cinctus between pre- and postsclerites. Oblique mesopleural sulcus absent ( Fig. 6C )………………………… Dorylinae (part, Leptanilloides genus group)

11 Oblique mesopleural sulcus present ( Fig. 6D ). Mandibles triangular………… Proceratiinae (part)

– Oblique mesopleural sulcus absent ( Fig. 6C ). Mandibles nearly linear ……………………………… ………………………………………………………… Ponerinae ( Ponerini part, Dolioponera )

12 Mandibles triangular, worker-like, with distinct and elongate masticatory margin ( Fig. 6E )… 13

– Mandibles reduced, linear, spatulate, or falcate, without distinct masticatory margin ( Fig. 6B , F–G) …………………………………………………………………………………………………… 16

13 Abdominal segment IV without cinctus between pre- and postsclerites ( Fig. 5C). Petiolar tergum and sternum completely fused in anterior third, without visible suture ( Fig. 6H ). Mandibular teeth robust………… Myrmeciinae , part ( Prionomyrmecini : Nothomyrmecia )

– Abdominal segment III with cinctus between pre- and postsclerites ( Fig. 5H). Petiolar tergum and sternum not insensibly fused in anterior third; if fused, suture visible along entire petiolar length ( Fig. 6I ). Mandibular teeth absent, fine, or robust…………………………………… 14

14 Metatibia with one ventroapical spur or prora thin and anteriorly directed, extending beneath helcium …………………………………………………………………………………………………… 15

– Metatibia with two ventroapical spurs and prora absent or thick and directed ventrally, not extending beneath helcium……………………………… Ponerinae ( Platythyreini : Platythyrea )

15 Crossvein 1m-cu present, thus discal cell 1 closed ( Fig. 7A ). Mandibles dentate; at least two teeth present on masticatory margin…………………………………… Ectaheteromorph clade

– Crossvein 1m-cu absent, thus discal cell 1 open ( Fig. 7B ). Mandibles edentate or masticatory margin produced apically as single tooth…………………… Proceratiinae (part, Discothyrea )

16 Mandibles falcate ( Fig. 6G ) to narrowly linear ( Fig. 11 A–B)……………………………… 17 – Mandibles nub-like ( Fig. 6F ), spiniform ( Fig. 6B ), or spatulate (broad in profile view)………… 18

17 Petiolar tergum and sternum clearly delineated. Anterior clypeal margin with ( Fig. 6G ) or without pegs. Abdominal segment III about same size as segment IV, metasoma after petiole well-sclerotized. Global……………………………… Amblyoponinae (excluding Apomyrma )

– Petiolar tergum and sternum smoothly fused (similar to Fig. 6H , but along entire petiolar length; note that longitudinal line on petiole in Fig. 11C is a carina unassociated with sclerotic margins). Anterior clypeal margin without pegs ( Fig. 11 A–B). Abdominal segment III slightly reduced relative to segment IV, although metasoma after petiole weakly sclerotized ( Fig. 11C ). Endemic to Amazon basin……………………………………………… Martialinae (Martialis)

18 Mesosoma anteriorly elongated: Mesonotum almost twice as long as broad in dorsal view, and lateral pronotal face longer in profile view than head in full-face view ( Fig. 7C ). Pterostigma absent. Petiole broadly attached to abdominal segment III, node weak. Afrotropical ……………………………………………………………… Amblyoponinae (part, Apomyrma )

– Mesosoma not anteriorly elongated: Mesonotum much less than twice as long as broad in dorsal view, and lateral pronotal face in profile view shorter than to as

long as head length in profile view ( Fig. 7D ). Pterostigma present or absent. Petiole very narrowly attached to abdominal segment III, node strong, except Simopelta (Neotropical) ………………………………………………………… Ponerinae ( Ponerini part)

19 Basimere strongly developed; distinct from and usually much larger than telomere. Telomere restricted to posterior apex of basimere, not or only slightly extending anteroventrally beneath basimere ( Fig. 7E ). Petiole narrowly or broadly attached to abdominal segment III. Masticatory margin of mandible often finely serrate. Antenna with 11–13 antennomeres…… Dolichoderinae

– Basimere weakly developed; usually indistinct from and usually about the same size as telomere. Telomere extending anteroventrally beneath basimere almost to base of paramere ( Fig. 7F ). Petiole narrowly attached to abdominal segment III. Masticatory margin of mandible never serrate. Antenna with 8–13 antennomeres……………………………………………………… 20

20 Forewing venation nearly complete: Mf3-4 and 2rs-m present, thus submarginal cell 2 closed ( Fig. 7A , SMC2). Marginal cell 1 extremely long, at least one-third chord length of wing. Petiolar peduncle long and slender; node short, dorsoventral height somewhat less than maximum diameter of posterior petiolar foramen ( Fig. 15C ). Sri Lanka ……… Aneuretinae (Aneuretus)

– Forewing venation reduced: Mf2-4 and 2rs-m absent, thus submarginal cell 2 open ( Fig. 7B ). Marginal cell 1 length less than one-third chord length of wing. Petiolar peduncle short to absent ( Fig. 16B ), not particularly slender when developed; node variable. Global………… Formicinae

Figures

Fig. 10. Representative males of Leptanillinae, lateral view A. Protanilla “TH01” (Thailand, CASENT0119776, A. Nobile), arrow indicates loss of abdominal segment II petiolation. B. Protanilla “TH03” (Thailand, CASENT0119791, E. Prado). C. Leptanilla swani (Australia, CASENT0172318, A. Nobile). D. Protanilla sp. (Indonesia, CASENT0178838, A. Nobile), arrow indicates basolateral basimeral process. E. Scyphodon sp. (Indonesia, MCZ155112w, A. Nobile). F. Noonilla sp., used with permission from Petersen (1968). Scale bars: A, C, E–F = 0.2 mm, D = 0.5 mm, B = 1.0 mm.

Fig. 4. Male morphology. A–C. Abdominal sternum IX in ventral view. B. Oblique. D–E. Petiole in lateral view. F. Forewing in dorsal view. G–H. Propodeum in lateral view. — A. Aenictogiton indet. (Zambia, CASENT0106126, M. Branstetter). B. Cerapachys “parasyscia” lineage (Kenya, B. Boudinot). C. Emeryopone buttelreepeni (Thailand, CASENT0278779, B. Boudinot). D. Paraponera clavata (?Panama, B. Boudinot). E. Cerapachys lividus (Madagascar, CASENT0138502, D. Raharinjanahary). F. Phaulomyrma indet. (Thailand, UCRENT150358, A. Nobile). G. Leptanillinae indet. (Thailand, CASENT0156249, B. Boudinot); arrow indicates dorsal margin of petiolar foramen. H. Adelomyrmex dentivagans; arrow indicates propodeal lobe. All scale bars = 0.2 mm, except D–E = 1.0 mm.

Fig. 6. Male morphology. A–B, E–G. Head capsule in frontal view. C–D. Mesosoma, lateral view. H–I. Petiole, ventrolateral view. — A. Probolomyrmex indet. (Madagascar, CASENT0080551, A. Nobile). B. Anochetus boltoni (Madagascar, CASENT0063847, A. Nobile). C. Leptanilloides gracilis (Guatemala, CASENT0234561, M. Borowiec). D. Odontomachus simillimus (Seychelles, CASENT0172666, A. Nobile). E. Platythyrea arthuri (Mayotte, CASENT0132466, E. Prado). F. Protanilla indet. (Thailand, CASENT0119776, A. Nobile). G. Stigmatomma indet. (Madagascar, CASENT0007087, E. Prado). H. Nothomyrmecia macrops (Australia, B. Boudinot). I. Neoponera cf. apicalis (Honduras, B. Boudinot). Scale bars: A, F–G= 0.1 mm, B = 0.2 mm, C = 0.25 mm, E, H–I = 0.5 mm, D = 1.0 mm.

Fig. 7. A–B. Forewing. A. Ventral view, gyne. B. Dorsal view, male. C–D. Mesosoma, lateral view, male. E–F. Paramere, lateral view, male. — A. Aneuretus simoni (Sri Lanka, CASENT0172259, A. Nobile). B. Nylanderia vividula (U.S.A., CASENT0058918, A. Nobile). C. Apomyrma stygia (Central African Republic, CASENT0086073, E. Prado). D. Anochetus boltoni (Madagascar, CASENT0063847, A. Nobile). E. Dolichoderus validus (Costa Rica, INB0003662427, B. Boudinot). F. Formica pacifica (U.S.A., JTLC000006350, B. Boudinot). Scale bars: A–C, E–F = 0.5 mm, D = 1.0 mm.

Fig. 11. Martialis heureka Rabeling & Verhaagh, 2008, male, photomicrographs. A. Head, frontal view. B. Head, anteroventral oblique view. C. Body, lateral view. D. Body, dorsal view. Scale bars: A–B = 0.2 mm, C–D = 0.5 mm.

Fig. 15. Male representatives of three subfamilies. A, D. Frontal view. B–C, E. Lateral view. — A–B. Pseudomyrmex holmgreni, Pseudomyrmecinae (Paraguay, CASENT0173758, A. Nobile). C. Aneuretus simoni, Aneuretinae, used with permission from Wilson et al. (1956). D–E. Technomyrmex difficilis, Dolichoderinae (Madagascar, CASENT0049968, A. Nobile). Scale bars: A, D = 0.2 mm, B = 1.0 mm, E = 0.5 mm, no scale available for C.

Fig. 16. Male representatives of three subfamilies. A–B. Formica wheeleri, Formicinae (U.S.A., CASENT0173024, A. Nobile). C–D. Rhytidoponera, Ectatomminae, ectaheteromorph clade (Australia, CASENT0004610, A. Nobile). E–F. Pogonomyrmex rastratus (Argentina, CASENT0172673, A.