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The Exocrine System of Aneuretus Simoni (Formicidae, Aneuretinae)

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The Exocrine System of Aneuretus Simoni (Formicidae, Aneuretinae) ASIAN MYRMECOLOGY Volume 9, e009011, 2017 ISSN 1985-1944 | eISSN: 2462-2362 © Johan Billen DOI: 10.20362/am.009011 The exocrine system of Aneuretus simoni (Formicidae, Aneuretinae) Johan Billen Zoological Institute, University of Leuven, Naamsestraat 59, box 2466, B-3000 Leuven (Belgium) Corresponding author: [email protected] ABSTRACT. This paper reviews the morphology of the 11 exocrine glands that we found in Aneuretus simoni workers. In comparison with their stingless sister group Dolichoderinae, the stinging A. simoni has a well-developed venom gland with long and slender secretory filaments. They also share the occurrence of Pavan’s gland as source of the trail pheromone, although this gland has a bilobed appearance in Aneuretus, while it only has one lobe in dolichoderine species. The intramandibular gland is well-developed, while the metapleural gland has the lowest number of secretory cells known in ant workers. All glands described occur in both minor and major workers, with sometimes clear differences between both worker castes. Major workers have larger propharyngeal glands, which can be understood by their presumed role in food storage in the colony, and also have metapleural glands with twice as many secretory cells than minor workers. Minor workers in turn have a more developed venom gland, which is in line with their higher activity in nest defence and prey capture. Keywords: Aneuretus simoni, Aneuretinae, exocrine glands, morphology, histology, ultrastructure INTRODUCTION make A. simoni a vulnerable ant species, which has led to its inclusion in the IUCN Red List as Aneuretus simoni Emery, 1893 is the sole liv- ‘endangered’ (Fellowes & Brühl 2009). ing representative of the subfamily Aneuretinae, Information on the biology of A. simoni which is the sister group to the Dolichoderinae. has mainly been provided by the studies of Wilson This phylogenetic position is well-supported et al. (1956), Traniello and Jayasuriya (1981a,b, and based on morphological, fossil and molecu- 1985) and Jayasuriya and Traniello (1985). From lar data (Ward et al. 2010; Ward 2014, and ref- these papers we know that the small colonies are erences therein). The species is endemic to Sri polydomous and contain one or sometimes more Lanka, where it lives in pieces of rotting wood dealate queens, an average of 65 minor workers on the ground in forests of the wet and intermedi- and 2 (Wilson et al. 1956) or 3 (Jayasuriya & ate zones in the southeastern parts of the country Traniello 1985) major workers (but note that the (Wilson et al. 1956; Dias et al. 2011, 2013; Dias colony fragment we had available for the present & Ruchirani 2014; Dias & Udayakantha 2016). study contained 4 major workers !). The worker This very limited geographical distribution to- caste is clearly dimorphic with no intermediate gether with its unique phylogenetic position individuals between the minor and major workers 2 Johan Billen (Wilson et al. 1956; based on this paper, we here glands of A. simoni, together with novel histolog- also refer to the large workers as ‘majors’ rather ical and ultrastructural data on the other glands, than ‘soldiers’). Morphometric data on minor and that had not yet been studied before. major workers as well as queens are given in Dias (2014), and include head width measurements of 0.44-0.51 mm for minor workers, 0.61-0.86 mm MATERIAL AND METHODS for major workers, and 0.82 mm for queens. The major workers do not participate in During a short visit to Gilimale Forest in south- brood care or colony defence, but show a high ern Sri Lanka in December 1986, we found a nest activity during nest moving, when they lay trails fragment of Aneuretus simoni in a decomposing and transport brood and workers. Majors also fallen twig. This sample contained 16 minor and show a high rate of trophallaxis with both adult 4 major workers, of which 13 minors and 2 ma- and callow minor workers, and therefore may jors were prepared for sectioning (light and elec- play a role in food storage (Traniello & Jayasuriya tron microscopy), the remaining 3 minors and 2 1985). Mature minor workers, on the other hand, majors were prepared for scanning microscopy. are mainly in charge of nest defence, while cal- The latter were mounted on stubs and coated low minors in such situations retreat with brood with a thin layer of gold before examination in a towards the nest interior (Traniello & Jayasuriya JEOL JSM-6360 scanning microscope. For sec- 1985). The callow workers are also involved in tioning, workers were separated into head, thorax queen-related acts, brood care and foraging. This and abdomen, these tissues were then fixed in 2% early foraging is explained in the species’ food glutaraldehyde, buffered at pH 7.3 with 50 mM habits, in which insect prey is directly offered to Na-cacodylate and 150 mM saccharose, and post- the larvae (Wilson et al. 1956), thus making the fixed in 2% osmium tetroxide. After dehydration otherwise unrelated tasks of foraging and larval in a graded acetone series, tissues were embedded provisioning part of the same behavioural se- in Araldite. Serial semithin sections with a thick- quence (Traniello & Jayasuriya 1985). It is note- ness of 1 µm were made with a Leica EM UC6 worthy that callow minor workers are “unusu- ultramicrotome, stained with methylene blue and ally active in foraging-related tasks” (Traniello & thionin, and examined with an Olympus BX-51 Jayasuriya 1985). During prey capture, the ants light microscope. For ultrastructural analysis, we use their well-developed sting. They are not ex- studied thin sections of 70 nm thickness, double clusive predators, however, as they also collect stained with uranyl acetate and lead citrate, under carbohydrates from rotting fruit (Jayasuriya & a Zeiss EM900 electron microscope. Traniello 1985). The presence of a sting clearly distinguishes Aneuretus from the Dolichoderinae, although the detailed anatomy of the sclerites of RESULTS AND DISCUSSION the venom apparatus with the furcula fused to the anterior sting base in both groups supports the The following survey includes a description of very close relationship between Aneuretinae and the 11 exocrine glands that we found during the Dolichoderinae (Blum & Hermann 1978). examination of our serial sections (Fig. 1). Ac- Studies on the exocrine system of A. cording to the commonly used classification of simoni have been given in brief anatomical de- insect exocrine glands by Noirot and Quennedey scriptions of the pygidial and Pavan’s gland, (1974), glands are either formed by simple epi- together with a documentation of their respec- thelial cells (class-1) or are formed by structurally tive functions in alarm communication and trail more complex bicellular units (class-3), of which laying (Traniello & Jarasuriya 1981). We added each unit comprises a secretory cell and a duct more detailed reports on the intramandibular cell. The connection between both cells is known gland (Billen & Verbesselt 2016a), Pavan’s gland as the end apparatus, that serves as a draining (Billen & Verbesselt 2016b) and the metapleu- device to guide the secretion from the secretory ral gland (Billen 2017). In the present paper, we cells via the duct cells to the exterior. The vari- bring a review on all previously studied exocrine ous glands will be shown in the order from head The exocrine system of Aneuretus simoni 3 Fig. 1. Profile drawing of a minor worker with indication of the various exocrine glands (drawn to scale). to abdomen. All longitudinal section figures are function in substrate marking and nestmate re- shown with the anterior side to the left. cruitment (Roux et al. 2010), which is the only case in which the function of the intramandibu- 1. Intramandibular gland lar gland is known. A special kind of class-3 in- Both minor and major workers show a clear intra- tramandibular gland has been found in Tatuidris mandibular gland with class-3 cells (Fig. 2A,B). tatusia, as the ducts of all secretory units cluster In both castes, approx. 8 cells open through the together in one main bundle, that opens through proximal upper surface of each mandible, while a single sieveplate at the ventral proximal side approx. 12 cells open through the proximal lower of each mandible (Billen & Delsinne 2014). The surface. The round to polygonal cells have a di- structural complexity of intramandibular glands ameter of 16.6 ± 2.7 µm in minor and 15.6 ± 2.7 is further illustrated by the existence of class-1 µm in major workers. Ultrastructural examina- glands as well. Epithelial intramandibular glands tion of the secretory cells reveals the presence of underneath the ventral mandibular surface have a well-developed granular endoplasmic reticulum been found in some Pachycondyla species (Mar- and Golgi apparatus, which is indicative for the tins & Serrão 2011) and Protanilla wallacei elaboration of a proteinaceous, and hence non- (Billen et al. 2013). Still another epithelial in- pheromonal secretion. More details can be found tramandibular gland has recently been described in Billen and Verbesselt (2016a). in Brachyponera sennaarensis, where it is asso- Class-3 intramandibular glands are ciated with the peculiar mandibular pit that is a commonly found in ants, and were first described diagnostic characteristic for this genus (Billen & by Schoeters and Billen (1994). The secretory Al-Khalifa 2016). cells discharge their contents mainly through tiny The intramandibular gland in A. simoni pores onto the upper mandibular surface via their is special as its class-3 cells open through both corresponding duct cells, as has also been found mandibular surfaces, and even more through the in Polyergus rufescens (Grasso et al. 2004) and lower surface. In other ants, class-3 intramandib- in Atta laevigata (Martins et al. 2015). In Oeco- ular glands mainly open through the upper sur- phylla longinoda, the gland cells open both at the face (Schoeters & Billen 1994; Roux et al.
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