Research Article |
Corresponding author: Enrico Schifani ( enrsc8@gmail.com ) Corresponding author: Mattia Menchetti ( mattiamen@gmail.com ) Academic editor: Brendon Boudinot
© 2023 Enrico Schifani, Antonio Alicata, Lech Borowiec, Fede García, Vincenzo Gentile, Kiko Gómez, Elia Nalini, Fabrizio Rigato, Sämi Schär, Antonio Scupola, Roger Vila, Mattia Menchetti.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Schifani E, Alicata A, Borowiec L, García F, Gentile V, Gómez K, Nalini E, Rigato F, Schär S, Scupola A, Vila R, Menchetti M (2023) Unrecognized for centuries: distribution and sexual caste descriptions of the West European Aphaenogaster species of the subterranea group (Hymenoptera, Formicidae). ZooKeys 1153: 141-156. https://doi.org/10.3897/zookeys.1153.98297
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There are only two Aphaenogaster species from the subterranea group in the western Mediterranean: A. ichnusa Santschi, 1925, from south-western Europe, and A. subterranea (Latreille, 1798), also occurring in central and eastern Europe. Historically, the two species have been widely misunderstood: A. ichnusa was long considered a Sardinian endemic subspecies of A. subterranea, while its continental populations were misidentified as A. subterranea s. str. Recently, A. ichnusa was elevated to species rank and its worker caste was redescribed with that of A. subterranea, allowing for their correct identification. Yet their distribution was documented in detail only for France and Sardinia. Furthermore, no morphological characters were described to distinguish the males and queens of the two species. By investigating private and museum collections, 276 new records of A. ichnusa are provided here and 154 of A. subterranea from the western Mediterranean. Additionally, qualitative and quantitative morphological characters were combined to identify their males and queens. We present the new southernmost, easternmost, and westernmost distribution limits for A. ichnusa. Based on our results, this species is widely distributed in Italy and Catalonia (Spain), also occurring on several Mediterranean islands, avoiding areas with continental climate and high altitudes. Sicily is the only island to host the less thermophilous A. subterranea, which otherwise extends westward to Galicia (Spain). Sympatric occurrence is not rare along the contact zone. Additional natural history observations are reported regarding foraging habits, associated myrmecophiles, habitat preferences, and colony structure in the two species.
Ants, Aphaenogaster ichnusa, biogeography, Mediterranean, Myrmicinae, Stenammini
The genus Aphaenogaster Mayr, 1853 belongs to the myrmicine tribe Stenammini Ashmead, 1905 (
The subterranea group currently includes eight species [A. epirotes (Emery, 1895), A. holtzi (Emery, 1898), A. ichnusa Santschi, 1925, A. kurdica Ruzsky, 1905, A. lesbica Forel, 1913, A. maculifrons Kiran & Aktaç, 2008, A. subcostata Viehmeyer, 1922, A. subterranea (Latreille, 1798)], mostly residing in the eastern Mediterranean and Caucasus region, where several putative undescribed species also exist (
Only two species belonging to the subterranea group are recognized in West Europe: A. subterranea (Latreille, 1798) (terra typica: mainland France) and A. ichnusa Santschi, 1925 (terra typica: Sardinia). The first was described using the spelling “subteranea” (
Aphaenogaster subterranea has a wide distribution, from Iberia to Anatolia, and north to central Europe, while the range of A. ichnusa is restricted to West Europe and does not occur in the Balkans (Borowiec and Salata pers. comm., 2022; MM unpublished data). Until recent years A. ichnusa was considered as a Sardinian endemic and a subspecies of A. subterranea. Their separation as two distinct species was only recently demonstrated based on worker morphology and mitochondrial DNA (
The investigation of specimens from private and museum collections allowed us to gather reliable distribution data of A. ichnusa and A. subterranea from the west Mediterranean basin, and to fill the current gaps of knowledge. Among them, we investigated several complete nest samples allowing us to morphologically characterize the sexual castes of the two species and provide tools for their identification.
In this study, we focused our investigation on the West European region, where A. ichnusa is present and co-occurs with A. subterranea. We re-identified worker specimens belonging to the subterranea species group found in the authors’ personal collections and the Natural History Museum of Milan. Specimen identification was performed using the morphological characters illustrated by
Queens and males associated with identified workers were examined to detect further distinctive morphological features. In total, we studied 16 queens from nine colonies and 17 males from seven colonies of A. ichnusa, as well as 16 queens from eight colonies and 19 males from nine colonies of A. subterranea. Samples were chosen from across the study region and included specimens from their terrae typicae (see Suppl. material
PrW Males only. In dorsal view, maximum width of the dorsal plate of the propodeum at the level of the propodeal spiracles.
SPWI Males only. In dorsal view, maximum width of the dorsal plate of the propodeum at the level of the propodeal spiracles.
MCMssctm Queens only. In dorsal view, quantification of stickman-like or reticulate microsculpture units on the mesoscutum: the number of connected lines building units and being separated by line intersections and by flections angled > 30° is counted. Very short lines are also considered full counts. Arithmetic means of three units per specimen are taken.
In addition to means to distinguish males and queens of A. ichnusa from those of A. subterranea, we provide identification keys that tell them apart from the other Aphaenogaster species occurring in the study area (i.e., A. cardenai, A. italica, A. ovaticeps, and species from the crocea, gibbosa, pallida, splendida, and sardoa groups; see
All characters are given in μm as mean ± sd (min, max). A complete list of the investigated material and of the morphological data is provided in the Suppl. material
Compared to A. subterranea, A. ichnusa is characterized by a different propodeal shape with relatively well-developed dentiform spines, as opposed to slight edges. This difference can be appreciated both in lateral view (as the spines protrude backwards from the propodeal profile and are often preceded by a gibbous form in the distalmost part of the propodeal dorsum) and in dorsal view (as the spines are wider than the remaining propodeum). Consequently, the SPWI/PrW ratio was found to be very different between the two species, with no overlap: 1.36 ± 0.14 (1.12, 1.58) in A. ichnusa, 0.911 ± 0.06 (0.80, 0.99) in A. subterranea (Fig.
Compared to other sympatric species of the same genus, A. ichnusa and A. subterranea can be distinguished based on the following combination of characters: shiny integument, mesosoma lacking a pronounced contrast between the anterior gibbosity of the mesosoma and the flat propodeum, the dorsal profile of the propodeum in lateral view relatively short and horizontal, forming approximately a 90° angle with the posterior profile, the rather elongated head shape, the body pigmentation pale to dark brownish.
The following traits are shared by the two species: the head, including mandibles, forms a subtriangular shape; its edges are rounded, and the head capsule is clearly longer than wide. Very large ovoidal compound eyes (~ ½ length of the head capsule) that significantly protrude out of the head capsule, well-distanced from three large ocelli. Mandibles dentate, ~ ½ length of the head capsule, their external side mostly straight for more than ¾. Clypeus medially slightly emarginated. Mesosoma clearly wider than the head, characterized by a well-developed anterior gibbosity. Propodeum much shorter than the remainder of the mesosoma. The horizontal section of the propodeal profile is shorter than its two vertical sections (anterior and posterior), which both form angles of ~ 90° with it. A ventral cuticular process protrudes from the metasternum. Long pedunculate petiole, globose postpetiole, the petiole and postpetiole have a similar heigh, while the postpetiole is wider than the petiole. The legs are long, with hind femurs approximately the same length as the entire mesosoma. The antennae comprise of 11 flagellomeres, the scapi are short, measuring ca. twice the pedicel, and approximately extending slightly beyond the eyes if aligned perpendicularly to the head length axis. Body color pale to dark brown, appendages whitish. Surface sculpturing mostly weak, most of the ant is smooth and shiny, with at most isolated stickman-like units, very feeble rugae or reticulate microsculpture near the sutures, and feeble reticulate microsculpture on the head. Sparse erect and suberect setae mostly occur dorsally over the head, mesosoma and nodes, and both dorsally and ventrally on the first gastral segment and on the distalmost margins of the remaining segments, while shorter suberect or appressed setae cover the appendages.
The following key is meant to facilitate this distinction in the examined region. However, the intraspecific morphological variation of several species is still little known, so we recommend a careful approach in its use.
1 | Notably pronounced contrast between the anterior gibbosity of the mesosoma and a long and relatively flat propodeum, as better observed in lateral view; head less elongated |
A. italica Bondroit, 1918, A. sardoa (Mayr) (only Sardinia and Sicily), A. splendida (Roger, 1859), A. gibbosa (Latreille, 1798) or crocea group (only Sicily and southern Italian peninsula), i.e., A. fiorii Emery, 1915, A. sicula Emery, 1908, A. strioloides Forel, 1890, or A. trinacriae Alicata & Schifani, 2019 (see |
– | Propodeum much shorter and not as flat | 2 |
2 | Body color blackish; integument either most extensively matt, or mostly smooth and shiny and paired with a wide subrectangular head, or with reticulate microsculpture on the head and visible striae on the mesosoma and petiole |
remaining A. sardoa group species (see |
– | Body color ferruginous to dark brownish, integument largely smooth and shiny, without strongly developed surface sculpturing | 3 |
3 | Iberia only, very large size (approximate body length 6–6.8 mm) |
A. cardenai Espadaler, 1981 (see |
– | Combination not as above | 4 |
4 | Propodeal dorsum in profile view longer and inclined at ~ 45° before reaching the propodeal spiracle, lacking a clearly horizontal component |
A. dulcineae Emery, 1924, A. finzii Müller, 1921, A. ovaticeps (Emery, 1898), or A. pallida (Nylander, 1849) ( |
– | Propodeal dorsum shorter and more vertical, with a clear horizontal component |
A. ichnusa or A. subterranea (discrimination possible based on propodeal shape, see characters illustrated in the second paragraph of this section and Figs |
Queens of A. ichnusa and A. subterranea are much more difficult to tell apart based on their general shape as compared to workers and males. However, a subtle but very reliable character was found in the surface microsculpture of the dorsal mesosoma: in A. ichnusa, stickman-like reticulations occur sparsely and are modestly developed, while in A. subterranea they are visibly more developed and sometimes single stickman-like complexes may connect to each other covering very large areas. MCMssctm ranges do not overlap between the two species, while A. subterranea shows a high variation in the upper range: 4.33 ± 0.78 (3.00, 5.33) in A. ichnusa, 24.68 ± 22.97 (8.67, 87.67) in A. subterranea (Fig.
Compared to other sympatric species of the same genus, A. ichnusa and A. subterranea can be distinguished based on the following combination of characters: large mesosoma with wide smooth and shining patches, dark brown to ferruginous pigmentation with blackish areas, body setae relatively sparse, thick propodeal spines and mostly vertical propodeum lateral profile.
The following traits are shared by the two species: The head capsule forms a subrectangular shape, with rounded edges, and is as approximately as long as wide or slightly longer than wide. Large compound eyes (their length ~ ⅓–¼ of the head length) slightly protruding out of the head capsule. The distance between the central among the three ocelli and the level of the compound eyes is ca. the length of the ocellus itself. Mandibles dentate, ~ ½ length of the head capsule, their external side mostly straight for over ¾. Clypeus medially slightly emarginated. Massive mesosoma, slightly wider than the head. Propodeal spines well developed and straight, in profile view the of the propodeum is steep, with the section above the spines slightly inclined and the section below entirely vertical. Long pedunculate petiole, globose postpetiole, the petiole and postpetiole have a similar heigh, while the postpetiole is wider than the petiole. The antennae comprise ten flagellomeres, the scapi are moderately long, surpassing the posterior margin of the head if aligned parallel to the head length axis, while the antennal club consists of four flagellomeres and the flagellomeres 3–8 are only slightly longer than wide. Body color normally not uniform, ferruginous to very dark brown, with blackish patches usually occurring on the frons and paler orangish areas near the sutures of the mesosoma. Appendages pale orange to ferruginous. Rugose sculpture on most of the head, partly on the sides of the mesosoma including the entire propodeum, and on the nodes. The remainder of the body is smooth and shiny, except for stickman-like microsculpture. Abundant erect or suberect setae cover the head, the dorsum of the mesosoma and nodes, the first gastral segment, and the distalmost margins of the remaining segments, while shorter suberect or appressed setae cover the appendages.
The following key is meant to facilitate this distinction in the examined region. However, the intraspecific morphological variation of several species is still little known, so we recommend a careful approach in its use.
1 | Mesosoma matt and smaller, not hosting properly developed flight muscles, all species suspected to be incapable of normal flight dispersal |
sardoa group (see |
– | Mesosoma with wide smooth and shining patches and larger | 2 |
2 | Propodeum longer, its dorsal profile inclined at ~ 45°, propodeal spines thinner, body color uniformly ferruginous |
A. ovaticeps
(see |
– | Character combination deviating | 3 |
3 | Body color blackish, striate sculpture on the posterior part of the mesoscutellum and on the metanotum, only near the Italian border with Slovenia | A. epirotes (Müller, 1923) |
– | Color paler, mesoscutellum without striae | 4 |
4 | Body color uniformly very dark brown to blackish, flagellomeres more elongated, head with more parallel sides giving the impression of a more rectangular shape |
A. italica, A. gibbosa, A. ulibeli (see |
– | Body color paler, head sides not as parallel and more convergent frontad | 5 |
5 | Very hairy, comparatively dense setae at least on the gaster and postpetiole |
A. pallida group (A. dulcineae, A. finzii, or A. pallida, see |
– | Setae sparser | 6 |
6 | Body pigmentation yellowish or uniform ferruginous with at most a darkened area on the frons |
either crocea group (only Sicily and southern Italian peninsula), i.e., A. fiorii, A. sicula, and A. trinacriae, or A. splendida which is normally also characterized by a black transversal band on the first gastral tergite ( |
– | Body pigmentation overall darker and more irregular, blackish patches on the mesosoma and frons |
A. ichnusa or A. subterranea (discrimination possible based on microsculpture, see characters illustrated in the second paragraph of this section and Figs |
Note: The queens of A. cardenai and A. strioloides are currently unknown and, therefore, they are not included in this key. The first only occurs in Iberia and, considering that its workers are unique among West Palearctic Aphaenogaster and that queens usually retain a number of characters of workers, they are highly unlikely to be confusable with species of the subterranea group (
We recovered a total of 274 new records of A. ichnusa, and 154 of A. subterranea from the study area. We increased the know number of cells of 0.2 decimal degrees (ca. 22 km) occupied by A. ichnusa by 145% (103 new compared to 71 from literature) and of those occupied by A. subterranea by 64% (130/202). The two species showed a parapatric distribution, with only 4.5% of the cells (22/484) occupied by both species (Fig.
We report A. ichnusa for the first time for several islands and archipelagos: some of the Aeolian Islands (Lipari, Vulcano, Salina, Filicudi, Panarea), the Balearic Islands (Mallorca), the Maddalena Archipelago (Caprera), the Phlegrean Islands (Ischia, Procida), Tavolara island, the Tremiti islands (San Domino), and the Tuscan Archipelago (Capraia, Elba, Giglio, Montecristo).
The morphological distinction of the subterranea group species in the region is relatively easy (
While A. ichnusa inhabits areas with a Mediterranean climate, A. subterranea in the same region occurs only at higher elevations or in specific microclimates. However, A. subterranea is frequent at the sea level in continental climatic zones where A. ichnusa is absent (e.g., most of mainland France, the Po Plain). We show that A. ichnusa is frequent across a vast region of the western Mediterranean (
Notably, both A. ichnusa and A. subterranea seem to have a more limited distribution in Iberia, where they seem to be restricted to northern Spain. The reliability of few old records from southern Spain appears doubtful in the absence of more recent findings (e.g.,
Colonies of A. ichnusa and A. subterranea are often found nesting under rocks, and both species may be especially abundant in shady forest habitats with sufficient humidity and leaf litter (
However, despite their ecological success and wide distribution, still relatively little is known ca. the habits of these species besides anecdotal reports. They are probably mostly predators and scavengers, but at least A. ichnusa was also observed by the authors to tend root aphids, suggesting that trophobiosis may also play an important role in the diet of both. In addition, we observed isopods (Platyarthrus sp.), oribatid mites, silverfish, leaf beetle larvae (Chrysomelidae: Clytrinae), and planthoppers nymphs (Cixiidae) in A. ichnusa nests, and isopods (Platyarthridae in A. subterranea nests, in which also Cixiidae were reported by
Some of us also observed cooperative food transport in A. subterranea at least. Furthermore, A. subterranea workers are known to use tools: they drop small debris into liquid food and transport food-soaked tools back into their nest (
An integrative approach is needed to clarify whether hybridization or introgression between the two species have a significant role as observed in other ants (
We are grateful to Rumsaïs Blatrix for sharing with us the raw species distribution data used by
Support for this research was provided by “la Caixa” Foundation (ID 100010434) to Mattia Menchetti (grant LCF/BQ/ DR20/11790020).
Distribution data of Aphaenogaster ichnusa and A. subterranea
Data type: table (excel document)