Bert Hölldobler, Robert Stanton, and Hiltrud Engel.
A New Exocrine Gland in Novomessor (Hymenoptera: Formicidae) and Its Possible Significance as a Taxonomic Character.
Psyche 83(1):32-41, 1976.

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A NEW EXOCRINE GLAND IN NOVOMESSOR
(HYMENOPTERA: FORMICIDAE) AND ITS POSSIBLE SIGNIFICANCE AS A TAXONOMIC CHARACTER
BY BERT HOLLDOBLER, ROBERT STANTON, AND HILTRUD ENGEL Department of Biology, Harvard University, MCZ Laboratories, Cambridge, Mass. 021 38
The genus Novomessor is comprised of only three species: N. albisetosus, N. cockerelli and N. manni. The first two species are rather common in the Southwestern United Staes and North- ern Mexico (CREIGHTON 1950, 1955), and the latter has been col- lected along the Pacific coast of Mexico (KANNOWSKI 1954). The forms of Novomessor were originally described as Aphaeno- gaster, and recently W. L. Brown (1974) suggested that they should be placed back in that genus. He pointed out that "the characters supposed to distinguish the two genera are not very strong when one considers the whole world fauna of this complex". Brown's arguments were especially supported by his reexamination of Novomessor manni Wheeler and Creighton (1934) and Aphaeno- ggster ensifera Fore1 (1899), which he found to be synonymous. He concluded his reasoning by stating ". . .the example of A. ensifera and N. manni may help to alert myrmecologists to the kind of change to be expected of a worldwide reclassification. One of the changes in status resulting from this study is of course the return of cockerelli and albisetosus to their original generic assignment in Aphaenogaster".
In the course of a comparative study of communication mecha- nisims in Novomessor, we discovered a new complex exocrine gland. Since this gland is a very distinct character, it should be given con- siderable weight in the future taxonomic assessment of the species possessing it.
MATERIAL AND METHODS
Live specimens of N. albisetosus and N. cockerelli were collected in southern Arizona near Portal. For histological investigations the *~anus&ipt received by the editor June 15, 1976. 32
Pu&e Ìö3:32-4 (1976). hup ttpsychu einclub orgtS3/83-012 html



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I 9761 Holidobler, Stant on, and Engel- Exocrine Gland 33 Figure I
a) Sagittal section through the third and fourth tergite of a N, albiseiosus worker. b) Schematic drawing of the histological section, showing the glandular cells (GI, the glandular channels (CH), the cuticular cup structure (CU),and the intersegmental membrane [I) between the third and fourth segment.



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34 Psyche [March
F~gure 2. Sagittal section through the tergal gland complex, showing the chan- nels that open through the intersegmental membrane. ants were fixed in alcoholic Bouin (Dubosq Brasil), embedded in Methyl Methacrylate and sectioned 8 P with a Jung Tetrander I microtome (RATHMAYER IW), The staining was Azan (Heiden- hain). The SEM pictures were taken with an AMR 1000 A Scanning Electron Microscope. For comparative morphological studies of cuticular surface structures we used dry specimens of the ant col- lection of the Museum of Comparative Zoology of Harvard Uni- versity.
Whenever we dug up a nest of N. albisetosus we noticed a very repugnant odor. The same odor can be released when the gaster of a Novomessor worker is crushed. First we assumed that the substance originates either from the poison gland or the Dufour's gland or the hindgut, yet after all these organs were removed from the gaster the abdominal residue still exuded the odor strongly. Next we dissected segment by segment. In this way we finally de- termined that the odor was emanating from the third and fourth



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19761 Holldobler, Stanton, and Engel-Exocrine Gland 35 Table 1.
Species of ants which have been checked for the presence or absence of the cuticular cup structure. Except where noted, all ants that were looked at were workers.
With Structure:
Novomessor albisetosus Mayr (workers, males, and females) Novomessor cockerelli Andre (workers, males, and females) Ocymyrmex picardi Fore1
Without Structure:
Aphaenogaster crocea
subsp. sicula Emery
A ensifera Forel*
A. famelica F. Smith
A. flemingi M. R. Smith
A. fulva Roger
A. gibbosa Latreille
A. laevior Emery
A. lamellidens Mayr
A. longiceps F. Smith
A. loriae Emery
A. mariae Fore1
A. miamiana Wheeler
A. obsidiana var. epirotes Emery
A. osimensis
Aphaenogaster pallida
subsp. finzii Muller
A. phalangium Emery
A. poultoni Crawley
A. praedo Emery
A. pythia Fore1
A. rudis Emery
A. sagei Fore1
A. sardoa Mayr
A. spinosa Emery
A. splendida Roger
A. subterranea Latreille
A. swammerdami Forel
A. texana Emery
A. tennesseensis Mayr
A. testaceopilosa Lucas
Aphaenogaster tipuna Foral
A. treatae Fore1
A. uinta Wheeler
A. weigoldi Viehmeyer
Stenamma brevicorne Mayr
S. diecki Emery
S. manni Wheeler
5'. schmittii Wheeler
Pheidole dentata Mayr
P. (Ischnomyrmex) longipes F. Smith
Tetramorium sericeiventre Emery
Ocymvmex weitzeckeri Emery
0. weitzeckeri var. arnoldi Fore1
Cataglyphis albicans var. cubica Forel
Cataglyphis bicolor Fabricius
C. viatica Fabricius
Messor aciculatus Smith
M. aegyptiacus Emery
M. barbarus Linne
M. capitata Latreille
M. luebberti Forel
M. meridionalis Andre
M. sanctus Fore1
M. striaticeps Andre
M. barbarus structor Latreille
Veromessor andrei Mayr
V. lariversi M. R. Smith
V. pergandei Mayr
*Brown (1974) has shown that Novomessor manni Wheeler & Creighton is a synonym of this species.




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36 Psyche [March
tergal segment. From these results we hypothesized that a gland might exist between the third and fourth tergite, and which ap- parently cannot be spotted under a dissecting microscope. We therefore conducted a series of histological investigations which finally confirmed our suspicion. Workers of N. albisetosus and N. cockerelli possess two large glandular complexes, located bi- laterally under the third tergite (Fig. 1). One complex consists of approximately 50 single glandular cells, each of which sends an individual channel through the intersegmental membrane between the third and fourth tergite (Fig. 2). The external openings of these channels are closely associated with a series of cuticular "cups", which are located at the apical end of the dorsal surface of the fourth segment. Under the dissecting microscope the arrangement of the series of cups looks like a netlike structure, but the SEM pictures clearly reveal the hexagonal shape of the individual cups which are arranged like the cells of a honeybee comb (Fig. 3). Normally this part of the fourth tergite is tightly overlapped by the third ter- gite, and only by pulling the segments apart is the structure exposed. We assume that the cups serve as repositories for the glandular secretions. When the substance is needed the ant exposes this area and the chemical evaporates. Indeed, the odor can be released sim- ply by pulling the third and fourth tergite slightly apart. These tergal glands with the associated cuticular cup structure are found not only in the worker caste but also in queens and males (Fig. 4). In addition males of N. albisetosus and N. cockerelli were found to possess a similar glandular complex located bilaterally under the fourth tergite. The glandular channels open through the inter- segmental membrane between the fourth and fifth segment. The cuticular cup structure at the fifth segment is, however, much less conspicuous than that at the fourth segment.* In general, there appear to be no distinct differences in the tergal glands and the cup structures of N. albisetosus as opposed to N. cockerelli. Although we did not have fixed specimens of A. ensifera ( N. rnanni), the investigation of dried specimens in the systematic collection of the Museum of Comparative Zoology revealed that the *Another, previously undescribed exocrine glandular complex was found in workers and queens of N. albisetosus and N. cockerelli ventrally at the fourth seg- ment. The glandular channels open through the membrane near the cloaca. We are currently investigating the function of this gland.



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19761 Holldobler, Stanton, and Engel- Exocrine Gland 37 cup structure is missing in this species. Furthermore we surveyed 32 species of Aphaenogaster and 4 species of Stenamma, and in none of them could we find the cup structure (Tab. 1). An additional histological study of two Aphaenogaster species (A. texana, A. rudis) confirmed the absence of the tergal glands. It thus seems reasonable to suppose that the absence of the cup structure also indicates the absence of the tergal glands.
Although none of the investigated forms of Aphaenogaster and Stenamma possess the cup structure, we found a very similar cutic- ular structure in Ocymyrmex picardi (tribe Ocymyrmecini). This came as a surprise, because the species is taxonomically not at all close to Novomessor. In Ocymyrmex the structure is also located on the dorsal surface of the fourth tergite (Fig. 5). The "cups" do not have the same approximate hexagonal shape and they appear to be not as deep as those of Novomessor. Since we could not obtain fixed specimens, we are unable to say if the structure is also associated with tergal glands. With the possible exception of Ocymyrmexpicardi, where a simi- lar net-like structure was found at the fourth tergite, the newly dis- covered exocrine tergal glands seem to be restricted to the two species Novomessor albisetosus and N. cockerelli. They are absent in A. en- sifera ( = N. manni) and in all other investigated species of Aphaeno- vaster. Our findings seem therefore to support Brown's contention that N. manni should be reclassified as a species of Aphaenogaster. On the other hand, the existence of a large and rather complex exo- crine gland associated with a particular cuticular structure in N. albi- setosus and N. cockerelli(the type species of Novomessor) may argue against the assignment of the genus Novomessor to the synonymy of Aphaenogaster. It is clear that the repugnant odor, released by dis- turbed ants of N. albisetosus, originates from these tergal glands. We believe that the secretion's function is defense, although our experi- ments have not yet identified the kind of enemies against which the substance is directed. Only little is known about the natural product chemistry of Novomessor. Vick et al. (1969) found a series of hydro- carbons in Novomessor cockerelli, but they did not attempt to identi- fy the glandular source of these substances. However, they discuss rather vaguely the discovery of new abdominal glands: "A very large



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38 Psyche [Marc




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I 9761 Hdldobkr, Stant on, and Engei- Exocrine Gland Figure 4. The SEM picture of the fourth tergite of a male of N. albisetosus. glandlike structure, which we call the 'dorsal gland', occupied the dorsal part of the gaster above the digestive tract. It varied in size, but often it extended from the posterior to the anterior end of the gaster and from side to side. It was composed of countless small round yellow globules apparently connected by what may be glandular tissue". But then they write: "It is possible that what appeared to be glandular tissue was not that and the dorsal gland might be some type of fat body arrangement". Our histological investigation did not reveal any glandular type which would fit the description of the 'dorsal glands'. We believe that Vick et al. have indeed described the fat body tissue, but then it is hard to under- stand how the fat body can be mistaken for a new 'dorsal gland'. Figure 3 (opposite)
a) SEM picture of the gaster ofa N. albisefosus worker. The third tergite is slightly lifted and the net-like cup structure can be seen on the surface of the fourth tergite. b) Separated fourth tergite with the cup structure fully exposed. c) The SEM close up picture shows clearly the hexagonal cups.



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40 Psyche [March
Figure 5. .SEM picture of a dried specimen of a Ocyryvrmex picardi worker showing the net-like cup structure.
Even more confusing is the description of additional 'anal glands'. Vick et al, write: "In addition, there were several glands or reser- voirs which we call the *anal glands', that opened dorsally near or into the cloaca! opening. Each of these glands was composed of a few linearly arranged globules that became progressively smaller distally from their attachment near the anus. No other glandular tissue was seen attached to them and distally they seemed to float free in the haemolyph". This description does not at all fit the glandular complex we discovered ventrally at the last abdominal segment, but it is a rather accurate description of the ovaries. We would like to thank Mr. Ed Seling for his superb assistance during the SEM work. Dr. Barry Bolton (British Museum of Natural History, London) offered very valuable advice and sug- gested that we check Ocymyrmexpicardt. This work was supported by the NSF grants BMS 75-06447 and BMS-7412494.



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19761 Holldobler, Stanton, and Engel- Exocrine Gland 4 1 BROWN, W. L.
1974. Novomessor manni a synonym of Aphaenogaster ensifera (Hymen- optera: Formicidae). Ent. News, 85: 45-53. CREIGHTON, W. S.
1950.
The ants of North America. Bull. Mus. Comp. Zool. Haw. 104:l-585, 57 pi.
1955.
Studies on the distribution of the genus Novomessor (Hymenoptera: Formicidae). Psyche, Cambridge, Mass. 62: 89-97. FOREL, A.
1899. Insecta. Hymenoptera (Formicidae). Biologia Centrali-Americana 3: 1-160, 4 pi.
KANNOWSKI, P. B.
1954. Notes on the ant Novomessor manni (Wheeler and Creighton). Occas. Pap. Mus. Zool. Univ. Michigan 556: 1-6. RATHMAYER, W.
1962. Methylmethacrylat als Einbettungsmedium fur Insekten. Experientia 18: 47.
VICK, K., DREW, W. A., MCGURK, D. J., EISENBRAUN, E. J. AND WALLER, G. R. 1969. Identification of Hydrocarbons from Novomessor cockerelli. Ann. of the Entomol. Soc. of America 62(4); 723-725. WHEELER, W. M. AND CREIGHTON, W. S.
1934. A study of the ant genera Novomessor and Veromessor. Proc. Amer. Acad. Arts. Sci., Boston, 69: 341-387.




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