Tetramorium atratulum

A workerless social parasite of Tetramorium caespitum and Tetramorium impurum, and as reported by Lapeva-Gjonova et al. (2012) from Tetramorium moravicum in Bulgaria and Tetramorium chefketi, 1911 in Bulgaria and Turkey. This species is rarely encountered.

Identification
From Fisher and Cover (2007): The males are found only in nests of the host and are pupoidal - cream to yellow in color, wingless, and barely able to walk. The queens are tiny and physogastric when found in the host nest. When found outside the nest they are dispersing and may be recognized by the unique, prominent median longitudinal depression on the dorsal surface of the gaster.

Distribution
Spain to Central Siberia, North Italy to South Sweden, also North America (Collingwood 1979).

Distribution based on Regional Taxon Lists
Nearctic Region: United States. Palaearctic Region: Albania, Armenia, Austria, Belarus, Belgium, Bulgaria, Czech Republic, Denmark, Finland, France, Germany, Greece, Hungary, Iberian Peninsula, Italy, Latvia, Lithuania, Luxembourg, Netherlands, Poland, Republic of Moldova, Romania, Slovakia, Spain, Sweden, Switzerland, Turkey, Ukraine, United Kingdom of Great Britain and Northern Ireland.

Biology
This species exhibits a form of Social Parasitism.

Queens are most likely adopted in orphaned host colonies (Fisher and Cover 2007, Buschinger 2009). Queens and males mate in the nest. Sex ratios are female biased (Heinze and Buschinger 2007)

A. Buschinger was able to rear a parasitized colony that successfully produced sexuals, as reported here:

Wheeler (1908) described Anergates queens and males he found in nest during a 1907 visit to Europe. Not only does his account provide insights about this ant's biology, it is also an interesting account of Wheeler collecting, and experimenting with, ants with Forel.

"On only one occasion was I fortunate enough to find a colony of this rare, workerless parasite. June 6, at 2 P. M., while collecting near Vaud, in the very meadow in which Forel as a young man made many of his classical' observations for the "Fourmis de la Suisse", I discovered a medium-sized Tetramorium caespitum colony from which female Anergates were escaping in consideable numbers. The nest was around the roots of a plantain (Plantago major) and the females issued one by one from the entrances, climbed the leaves to their tips, and flew away in all directions over the sun-lit grass. At 3.30 P. M. Prof. Forel joined me and we excavated the nest with great care. It contained besides the obese mother queen of Anergates (Fig. Eb) and several hundred Tetramorium workers, more than a thousand winged queens (Fig. Ea), a few hundred of the wingless, pupa-like males (Fig. Ed), several pupae and a few larvee of the parasitic species. In the galleries of the nest dozens of couples were united in the act of mating. The Tetramorium workers picked up the single males and hurried away with them, but they paid little attention to the females. The colony was placed in a bag and on the following day used for experiments on Tetramorium colonies in Prof. Forel's garden at Chigny. On opening the bag the next morning, I found several of the Anergates in copila, but most of the females had either lost their wings or were ready to drop them at the slightest touch. Eight Tetramorium colonies that had large nests with multiple craters in the paths of the garden, were selected, and the females were placed near them, one at a time, on the ground. In all cases when they were placed within a few centimeters of the openings, they entered the nest almost immediately; when placed at a greater distance they wandered about demurely till they found an opening and then at once crept into it. Seven of the nests were thus entered by numbers of the queens without creating the slightest excitement among the Tetramorium workers. These merely stopped when they happened to meet a female, seized her by the wings, thorax or pedicel, but at once dropped her and went about their work. In no case was one of the queens injured. In three of these colonies they were seized by single workers and carried into the nest as fast as I could set them on the craters. Both males and females were placed near the openings of one of the nests. The males were seized with signs of keen interest and some animosity, to judge from the way in which the workers bent their gasters forward and tried to sting the helpless creatures. They were not killed, however, but carried a few decimeters from the nest and thrown away, sometimes from the top of a pebble or lump of earth. This was being done while other workers were carrying the females into the nest. One vigorous colony exhibited a different behavior. All the parasites, both male and female, were at once seized, pulled about by the legs, wings and antennae and then carried away and dumped on the ground at some distance from the nest. In this instance several of the parasites of both sexes were injured so that they could not walk. Strange Tetramorium workers placed on any of the nests above mentioned were suddenly pounced upon and killed. These observations show that the Anergates queens are, as a rule, treated with great lenity and even carried into the nests, but that the males are rejected. They also show that certain colonies are positively hostile to both sexes of the parasites. In all cases, however, the behavior of the Anergates queens was very uniform: they sought and entered the Tetramorium  nests as if these belonged to them, offered no resistance when seized and, when roughly handled, merely curled up and feigned death. The experiments were continued throughout the morning. With the gradually increasing temperature towards noon the Tetramorium workers became more numerous and active outside their nests but their treatment of the Anergates, which I was continually giving them, remained the same. Late in the afternoon the experiments were repeated with two of the colonies which during the morning had been entered without protest by a number of the parasitic queens. The workers were out in a multitude, excavating and dragging in insect food. When male, female or pupal Anergates were placed on these nests, the males and pupae were promptly seized and' thrown away and the females were also seized, but less promptly, and also rejected. Some of the latter that had managed to enter the nests were brought out and dumped at a distance of several decimeters from the entrances. I watched the nests for some time and although a few of the females were not brougnt out, I am, of course, unable to state whether they were subsequently adopted, killed in the galleries or ejected. It appears, therefore, that the acceptance of Anergates by the Tetramorium under natural conditions is not as immediate as the observations of Adlerz and Wasmann on artificial nests would lead one to suppose. The fact that Anergates is so rare an ant, although its sporadic colonies produce enormous numbers of females in regions inhabited by myriads of Tetramorium  colonies, shows that permanent adoption is not easily effected.''

Wheeler remarks in a footnote that Forel assessed the colonies in his garden the following year. He found sexual pupae of Tetramorium in every nest, showing that none of the queens had succesfully been adopted into the colonies.

Wheeler (1909) described finding two Tetramorium nests with about 1 km south of Zermatt, Switzerland "at an altitude of about 1,620 m., on the warm western slope of the Matter valley"

"August 13. A large Tetramorium colony under half a dozen rather large, flat, contiguous stones arrested my attention, because it, contained several hundred larvae, all of the same size and of a peculiar gray color, unlike the gleaming white larvae so abundant in the other colonies of this ant. On scrutinizing the superficial chambers of the nest more closely, I saw four fine, dealated Anergates queens in the peculiar, obese or physogastric condition, which this alone of all European ants is able to attain. Three of these queens were close together under the center of one of the stones, the other was in a similar position under an adjacent stone. It was quite clear then that the gray larvae were the offspring of these queens, and from their size it was evident that they were mature and nearly or quite ready to pupate. Of course, there were besides only Tetramorium workers in the colony and none Of their larvae. I do not know whether other observers have noticed the singular uniformity in the age and development of the larvae of Anergates. It is very striking, though it is what we should expect, for the life of the Anergates colony must be of short duration, since it cannot exceed that of its sterile host, the Tetramorium workers. It is, indeed, quite possible that the whole development of the Anergates colony does not require more than a year, or, at any rate, that the queens of this species become physogastric, owing to the rapid and enormous development of their ovaries, and begin to lay within a few months after entering the Tetramorium colony, and that the brood matures by the following summer. Owing to the altitude at which this colony was found (about 1,600 m.), the maturity of the brood must have been greatly delayed and probably would not have hatched till the latter part of August or early in September.

August 14. In the same locality but lower down the slope and less than a hundred meters from the Matter, I detected a second colony, which, however, was small and depauperate and was living under a single small stone. This colony, too, contained a number of the gray larvae, which, as in the preceding case, were all of the same size and partly adhering by means of their hooked, dorsal hairs to the lower surface of the stone. The nest also contained a number of large root~aphids of both sexes and in all their developmental stages. After careful search I found the obese Anergates queen, but she was dead and somewhat shriveled, and her thorax had been separated from her gaster."

Wheeler then goes on to offer some advice about how one might find Anergates atratulus:

"As collectors are always interested in the various parasitic ants that live with Tetramorium, I may here introduce a few suggestions that may aid them in detecting infested colonies. In the first place, it is advisable to concentrate one's attention on a locality in which Tetramorium colonies are unusually abundant. In the second place, the collector should examine the nests at the height of the breeding season, that is, during June and July at the lower, and early in August at the higher altitudes, when the normal colonies contain larvae and pUpie of all three phases. He may safely pass over at once all colonies containing the larger. male and female larvie and pupae of the Tetramorium, as such colonies do not contain Anergates and concentrate his attention on the colonies which at first glance appear to contain only workers and worker brood of the Tetramorium.

The presence of uniformly developed, gray larvae may be taken to indicate the occurrence of Anergates, if its presence is not already conspicuously indicated by the numerous imaginal brood of small black females and sordid yellow, nymphoid males. With a good pocket lens the Anergates larva may also be recognized by its peculiar hairs. I give a figure (Fig. 2, A) of a larva from one of the nests described above, and also of a mature worker larva of Tetramorium (Fig. 2, B) for comparison. It will be seen that though both larvae possess pairs of long anchortipped dorsal hairs, the head of the Anergates larva is naked, and its short dorsal and ventral hairs (b) are much more densely and compactly branching, while the longer hairs (a) are serrate and not branched at their tips like the homologous structures (d) of the Tetramori1tm larva. The anchor-tipped hairs (c) with sigmoid basal flexure are used in both species for fastening the larvie to the lower surfaces of stones, the roots of plants and the waIls of the galleries and chambers of the nest."

Castes
This species is a workerless parasite. Queens can become physogastric when reproductively active within a host nest. Males are degenerate, have no wings and are barely mobile.

Nomenclature

 *  atratulus. Myrmica atratula Schenck, 1852: 91 (q.m.) GERMANY. Wheeler, W.M. 1909g: 182 (l.). Combination in Tetramorium: Mayr, 1855: 429; in Anergates: Forel, 1874: 68 (see also p. 93). [Also described as new by Schenck, 1853: 186.] Senior synonym of friedlandi: Creighton, 1950a: 243. See also: Donisthorpe, 1915d: 89; Boven, 1977: 81; Wheeler, G.C. & Wheeler, J. 1955c: 128; Atanassov & Dlussky, 1992: 161.
 * friedlandi. Anergates friedlandi Creighton, 1934: 193 (q.) U.S.A. Junior synonym of atratulus: Creighton, 1950a: 243.

Queen
Creighton (1934), of the synonomized friedlandi - Length: 2.2 mm. (the gaster not expanded). Differing from the female of atratulus in the following characteristics: The single mucronate point with which the mandible is armed longer and stouter; the convex masticatory border of the mandible very feebly serrate (smooth in atratulus). Eyes nearly circular in outline and strongly convex with rather fine facets (oval and moderately convex with coarse facets in atratulus). Lateral ocelli small and so placed that they are hidden when the head is viewed from directly in front by the rectangular occipital crest on which they are borne (lateral ocelli larger and distinctly visible from the front in atratulus). Antennal scapes slightly and evenly curved outward, gradually increasing in thickness from base to apex and in repose surpassing the occipital border by an amount equal to the greatest thickness (in atratulus the scapes are almost straight, thickest at a point about three quarters of the distance to the apex and in repose surpassing the occipital border by an amount less than their greatest thickness). Seen from above the epaulet-like lateral portions of the pronotum are strongly concave, blunted behind and set off from the median portion of the pronotum by a rounded welt or ridge (in atratulus the lateral portions of the pronotum are only slightly concave, rather sharp behind and set off from the median portion of the pronotum by a sharp ridge). Scutum longer than in atratulus and with more overhang at the anterior edge. The posterior portion of the scutum is evenly depressed all the way across including the paraptera so that there is a sharp transition to the scutellum when the thorax is viewed in profile (in atratulus the depression of the scutum is median only, the paraptera not being depressed, so that there is a sort of a shallow trough formed on the dorsum of the thorax; however in profile the transition between the scutum and scutellum appears less abrupt because of the elevation of the paraptera above the level of the middle of the scutum). Scutellum narrower and much more convex than in atratulus. Epinotum seen from above with the lateral projections less prominent and more rounded than in atratulus. Seen from behind the broad longitudinal impression on the posterior face of the epinotum is broadly rounded above (narrower and rather pointed above in atratulus). Seen in profile the node of the petiole has a definite, short posterior face, a rounded and rather narrow summit and a long steeply sloping anterior face. Although both posterior anterior peduncles are short both are distinctly visible in profile and sharply set off from the node (in atratulus the node of the petiole is much bulkier with the dorsum broad and obtusely angular. The anterior and posterior peduncles are so short as to be virtually invisible when seen in profile). Postpetiole seen from above thinner from front to back than in atratulus with the anterior edge much less convex. The dorsum bears a shallow, median longitudinal sulcus (entire in atratulus). Abdomen with a deep median sulcus as in atratulus.

Sculpture very finely and evenly punctato-rugose except the very deeply notched clypeal border, the mandibles and the appendages which are shining. The sculpture is uniformly heavier than in atratulus, particularly on the posterior abdominal segments where it renders the surface definitely opaque (feebly shining in atratulus).

Color: head and thorax blackish brown, gaster a somewhat clearer brown, appendages dirty yellow. Wings hyaline, covered with numerous small hairs, the veins and stigma pale yellow.

Additional References

 * Adlerz, G. 1886. Myrmecologiska studier. II. Svenska myror och deras lefnadsförhållanden. Bihang till Kongliga Svenska Vetenskaps-Akademiens Handlingar. 11(18):1-329.
 * [[Media:Adlerz 1908.pdf|Adlerz, G. 1908. Zwei Gynandromorphen von Anergates atratulus Schenck. Ark. Zool. 5(2 2: 1-6) PDF]]
 * Buschinger, A., B. C. Schlick-Steiner, F. M. Steiner, and M. Sanetra. 2003. Anergates atratulus, eine ungewöhnlich seltene Parasiten-Ameise. Ameisenschutz Aktuell. 17:1-6.
 * Collingwood, C. A. 1979. The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomol. Scand. 8:1-174.
 * [[Media:Creighton 1934.pdf|Creighton, W. S. 1934. Descriptions of three new North American ants with certain ecological observations on previously described forms. Psyche (Camb.) 41: 185-200 PDF]]
 * Crawley, W. C. 1912. Anergates atratulus, Schenk., a British ant, and the acceptance of a queen by Tetramorium caespitum, L. Entomologist's Record and Journal of Variation. 24:218-219.
 * Fisher and Cover. 2007. Ants of North America. A guide to the Genera. University of California Press.
 * Heinze, J., B. Lautenschläger, and A. Buschinger. 2007. Female-biased sex ratios and unusually potent males in the social parasite Anergates atratulus (Hymenoptera: Formicidae). Myrmecological News. 10:1-5 PDF.
 * Schenck, C. F. 1852. Beschreibung nassauischer Ameisenarten. Jahrbuch des Vereins für Naturkdunde im Herzogthum Nassau Wiesbaden. 8:1-149.
 * Wheeler, W. M. 1908. Comparative ethology of the European and North American ants. J. Psychol. Neurol. 13:404-435, pl. III-IV.
 * Wheeler, W. M. 1909. Observations on some European ants. J. N. Y. Entomol. Soc. 17:172-187.