Occurrence and structural organization of the exocrine glands in the legs of ants

Apart from their obvious locomotory function and hence the presence of muscle fibres, ant legs are also endowed with an astonishing variety of exocrine glands. This paper reviews the presence and structural variety of the 20 different glands that have so far been found in the legs of ants. Four of these glands are described for the first time in this paper. Glands have been described in the three leg pairs, although considerable differences may exist. Glands occur in the various leg segments. A number of glands, especially those located in the hindlegs, may have a function in the production of trail pheromones. Other possible functions that have been reported deal with antenna cleaning, production of lubricant substances and sex pheromones.     

Tarsomere and distal tibial glands: Structure and potential roles in termites (Isoptera: Rhinotermitidae,Termitidae)

Social insects have numerous exocrine glands, but these organs are understudied in termites compared to hymenopterans. The tarsomere and distal tibial glands of the termites Heterotermes tenuis, Coptotermes gestroi and Silvestritermes euamignathus were investigated by scanning and transmission electron microscopy. Pore plates are visible in scanning micrographs on the distal tibial surfaces and on the ventral surface of the first and second tarsomeres of workers of H. tenuis and C. gestroi. In contrast, workers of S. euamignathus have isolated pores spread throughout the ventral surfaces of the first, second, and third tarsomeres and the distal tibia. In all three species each pore corresponds to the opening of a class-3 secretory unit, composed of one secretory and one canal cell. Clusters of class-3 glandular cells are arranged side by side underneath the cuticle. The main characteristics of these exocrine glands include their presence on all the legs and the electron-lucent secretion in the secretory cells. Possible functions of these glands are discussed.     

Survey of the exocrine system in Protanilla wallacei (Hymenoptera,Formicidae)

We studied the exocrine system of both workers and ergatoid queens of Protanilla wallacei using light, scanning and transmission electron microscopy. Our survey revealed the presence of 26 glands, of which 6 had never been found before in ants. Five of these represent novel discoveries for social insects in general. The overall novel discoveries comprise an epithelial stipes gland, a pharyngeal wall gland, a central petiole gland, a lateral postpetiole gland and a foot-sole gland in the hindleg pretarsi. The intramandibular epithelial gland was already reported in some bees previously, but is now for the first time also reported in ants. The exocrine system of workers and ergatoid queens is very similar, with only the spermathecal gland showing an obvious difference. This is in line with the limited anatomical as well as behavioural difference between both castes in Protanilla compared to the situation in Leptanilla.     

The leg exocrine system inSerritermes serrifer (Hagen, 1858), phylogenetic implications (Isoptera: Serritermitidae)

Summary The leg exocrine gland was examined in two species of Neotropical termites. Scanning microscopy studies showed a set of pores on the ventral surface of the first and second tarsomeres in all legs ofSerritermes serrifer. InHeterotermes tenuis these pores are present on a sunken plate in all castes. To date, this gland has been observed only in Rhinotermitid species. The presence of leg exocrine gland provides additional evidence supporting a close phylogenetic relationship between the Serritermitidae and Rhinotermitidae.     

Novel thoracic glands in the ant Myopias hollandi

Besides the common labial and metapleural glands, four novel exocrine glands are described in the thorax of both workers and queens of the ponerine ant Myopias hollandi. From anterior to posterior, these glands were designated as the propleural pit gland, the posterolateral pronotal gland, the anterolateral propodeal gland and the metasternal process gland. They all correspond with class-3 glands, that are made up of bicellular units that each comprise a secretory cell and a duct cell. In the propleural pit gland, the ducts are characterized by a gradually widening diameter, while in the three other glands the ducts show a portion which displays a balloon-like expansion, that on semithin sections stains very dark. For none of these novel glands the function is known as yet, although ultrastructural examination indicates that they produce a non-proteinaceous and therefore possibly pheromonal secretion.     

Queen Specific Exocrine Glands in Legionary Ants and Their Possible Function in Sexual Selection

The colonies of army ants and some other legionary ant species have single, permanently wingless queens with massive post petioles and large gasters. Such highly modified queens are called dichthadiigynes. This paper presents the unusually rich exocrine gland endowment of dichthadiigynes, which is not found in queens of other ant species. It has been suggested these kinds of glands produce secretions that attract and maintain worker retinues around queens, especially during migration. However, large worker retinues also occur in non-legionary species whose queens do not have such an exuberance of exocrine glands. We argue and present evidence in support of our previously proposed hypothesis that the enormous outfit of exocrine glands found in dichthadiigynes is due to sexual selection mediated by workers as the main selecting agents.     

An interommatidial exocrine gland with a “nail-headed” structure in the water strider Aquarius remigis (Hemiptera,Gerridae)

The fine structure of the interommatidial exocrine glands, found in the compound eyes of the water strider Aquarius remigis, is described using light, scanning, and transmission electron microscopy. The glandular pores of the glands are specialized into minute “nail-headed” structures (NS), which are described for the first time in arthropod compound eyes. Each NS is composed of two components: a rod-like stalk and a cup-like depression. The TEM study shows that the glands are class 3 epidermal glands as defined by Noirot and Quennedey (1974, 1991). Each gland consists of 3 cells: a gland cell, an intermediary cell, and a duct (canal) cell. The gland cell contains abundant electron-lucent vesicles, while the intermediary cell contains a large number of osmiophilic secretory granules. These two cells might secrete different substances which mix together in the dilated sac-like portion of the conducting canal before final release. The possible functions of the secretions released from these glands are discussed.     

Ca-dependent K channels in exocrine salivary glands

In the last 15 years, remarkable progress has been realized in identifying the genes that encode the ion-transporting proteins involved in exocrine gland function, including salivary glands. Among these proteins, Ca²⁺-dependent K⁺ channels take part in key functions including membrane potential regulation, fluid movement and K⁺ secretion in exocrine glands. Two K⁺ channels have been identified in exocrine salivary glands: (1) a Ca²⁺-activated K⁺ channel of intermediate single channel conductance encoded by the KCNN4 gene, and (2) a voltage- and Ca²⁺-dependent K⁺ channel of large single channel conductance encoded by the KCNMA1 gene. This review focuses on the physiological roles of Ca²⁺-dependent K⁺ channels in exocrine salivary glands. We also discuss interesting recent findings on the regulation of Ca²⁺-dependent K⁺ channels by protein–protein interactions that may significantly impact exocrine gland physiology.     

The function of the post-pharyngeal glands of the red imported fire ant, Solenopsis invicta buren

Using radiolabelled triglycerides and fatty acids we have shown that these 2 lipids are absorbed into the haemolymph of the imported fire ant, Solenopsis invicta Buren from the post-pharyngeal gland. The post-pharyngeal glands attain their greatest weight and contain the highest hexane extractable lipid in establishing queens which have just reared the first minum brood. The lipid content of the digestive system is greatest in queens initiating a mating flight with the majority of the lipid contained in the crop. During colony establishment by the queen the lipid content of the crop moves forward, some is fed to the developing larvae and some moves into the post-pharyngeal gland. The hexane extractable lipid from the postpharyngeal gland of newly mated queens consists of hydrocarbons, sterols. tri-, di-, and monoglycerides and free fatty acids with a trace of wax esters.Excision of the post-pharyngeal glands from mated established queens causes no noticeable change in their behaviour or the behaviour they elicit from the remainder of the colony. However, post-pharyngeal glandectomized females lost weight and died in ca. 2 months although their crop and midgut contained food. The post-pharyngeal glands therefore appear to function in much the same way as a gastric caecum.     

Diversity and morphology of abdominal glands in workers of the ant genus Myopias (Formicidae,Ponerinae)

Histological examination of serial sections through the abdomen of workers of three species of Myopias ants revealed the presence of several exocrine glands. These include the common venom and Dufour glands as well as the pygidial gland, but also more specific sternal glands and glands associated with the sting base and the gonostyli. Two of these glands have not been reported previously among ants: one is the paired oblong plate gland, that occurs next to the oblong plate and may have a pheromonal function. The other novel gland is the paired sting shaft gland, that occurs at the dorsal side in the proximal region of the sting shaft. A remarkable characteristic of these Myopias ants is that all glands of class-3 show ducts with gradually widening internal diameter. Myopias emeryi shows a clearly more simple variety of abdominal glands than Myopias maligna and M. sp.1.     

Dufour's gland secretion as a repellent used during usurpation by the slave-maker ant Rossomyrmex minuchae

In slave-making ants, the invasion of the host colony by newly mated queens is a critical stage. We studied the strategy used by Rossomyrmex minuchae queens to invade their host Proformica longiseta. Field observations revealed that queens enter the host nest unchallenged by the host workers in the vicinity of the nest entrance. Pre-usurpation queens were found to possess a highly inflated Dufour's gland, which considerably reduces in size after successful usurpation. Chemical analysis of these queen glands revealed tetradecanal to be the major product in pre-usurpation Rossomyrmex queens, but to be almost absent in queens that have been adopted by P. longiseta. We consequently hypothesized that tetradecanal is a repellent that is used by queens to prevent host worker aggression. We tested its repellent effect by attempting to deter starved, highly motivated workers from a droplet of honey. Tetradecanal indeed proved to be highly repellent both to host worker P. longiseta and non-host worker Formica selysi. It was even more powerful than limonene, a reported general ant repellent. These results are consistent with the hypothesis that R. minuchae queens use Dufour's gland secretion as a weapon during nest usurpation. The general use of tetradecanal as a defensive compound, and its seemingly non-specific repellent effect on ants, indicate that it may act as a general ant repellent. Its adoption by R. minuchae queens thus provides them with an efficient defensive and offensive chemical weapon during their long and risky search for new host nests.     

Female pheromone glands in arctiidae (lepidoptera). Evolution and phylogenetic significance

Few papers have been devoted to the female pheromone glands, phylogeny and high-level systematics of the Arctiidae. The diversity of these glands is here interpreted in the light of a revised classification. The presence, in the A8-A9 intersegmental membrane, of one or two, distinctly invaginated (‘saccular’), dorsal glands is a characteristic derived trait of the Arctiidae. Lithosiinae typically have an unpaired dorsal gland, anteriorly provided with a pair of short lobes. Non-lithosiine arctiids form a monophyletic group, in which the gland lobes are primarily very long. Several lineages can be characterized by the shape of their dorsal glands, notably the Ctenuchinae (inclusive of Euchromia), the Pericopinae and the Arctiini. Pheromone production is a well-established function of these dorsal glands, while the ventral, intersegmental ‘pouches’ observed in certain taxa may not be pheromone-producing structures. The Thyretini (here allocated to Syntominae) possess ventral saccular glands that bear a marked resemblance to the dorsal pair.     

Functional morphology and development of tibial organs in the legs I,II and III of the bushcricketEphippiger ephippiger (Insecta,Ensifera)

Summary The anatomy of the complex tibial organs in the pro-, meso- and metathoracic legs of adults and larvae of the bushcricketEphippiger ephippiger is described comparatively. The subgenual organ and the intermediate organ are differentiated in the same way in legs I, II and III; the anatomy of the crista acustica and the tracheal morphology are significantly different. The final number of scolopidia in the tibial organ of each leg is present at the time of hatching. In the subgenual organ, the number of scolopidia is the same in all legs; in the intermediate organ, and especially in the crista acustica, the number of scolopidia decreases from leg I to legs II and III. In the first larval instar, the morphology of the tibia, the course of the trachea and the anatomy of accessory structures are developed in the same way in each leg. The specific differentiations forming the auditory receptor organ in leg I, such as the acoustic trachea, the tympana and tympanal cavities, develop step by step in subsequent instars. The auditory threshold recorded from the tympanal nerve in the prothoracic leg of adults is remarkably lower than in the meso- and metathoracic legs. Morphometrical analyses of structures that are suggested to play a role in stimulus transduction on scolopidia of the crista acustica reveal significant differences in the three legs.     

Functional morphology of the postpharyngeal gland of queens and workers of the ant Monomorium pharaonis (L.)

Eelen D., Børgesen L.W. and Billen J. 2006. Functional morphology of the postpharyngeal gland of queens and workers of the ant Monomorium pharaonis (L.). —Acta Zoologica (Stockholm) 87 : 101–111 The postpharyngeal gland (PPG) is unique to ants and is the largest exocrine gland in their head. In queens of the pharaoh's ant, Monomorium pharaonis, the gland contains approximately 15 finger‐like epithelial extensions on each side and opens dorsolaterally in the posterior pharynx. In these ants the PPG morphology varies considerably according to age and mating status. The epithelial thickness increases with age and reaches a maximum at 3 weeks in both virgin and mated queens. A considerable expansion of the lumen diameter occurs in both groups between 4 and 7 days. Virgin queens release their secretion into the gland lumen from an age of 7 days, whereas mated queens accumulate large amounts of secretion in their epithelium. The increasing epithelial thickness, together with the increasing lumen diameter, the presence of numerous inclusions in the epithelium and the release of secretion, are indicative for increasing gland activity. The gland ultrastructure indicates involvement in lipid metabolism and de novo synthesis of lipids. The PPG of workers consists of 12 finger‐like tubes at each side. There is a significant difference in epithelial thickness between nurses and repletes and between nurses and foragers. We suggest the PPG serves different purposes in pharaoh's ants: it is likely that the PPG of workers and virgin queens is used to feed larvae. In mated queens the gland probably plays a role in providing the queen with nutritious oils for egg production. The PPG may also function in signalling species nestmate and caste identity, as well as in the reproductive capacity of the queens.     

Comparative morphology of cephalic exocrine glands among castes of the black ant Lasius niger

The glandular system is crucially involved in main aspects of ant social life. The function of glands has been primarily studied in the workers (the non-reproductive individuals in a colony). In contrast, little information is available on queens (the reproductive females in a colony) or males in spite of the obvious functional differences between these castes. Here we report a comparison of the general morphology of the mandibular, propharyngeal and postpharyngeal glands between the three castes of the black ant Lasius niger. The analysis clearly shows that all these cephalic glands differ in relative size between castes and suggests a link between gland structure and its behavioral role in queens, workers and males. In particular, males present a hypertrophied mandibular gland. This is consistent with the fact that these glands might be the source of the sex pheromone in this caste. By contrast, queens exhibited the most developed postpharyngeal glands. This is consistent with the production of particular cues by queens for workers to help them to distinguish between reproductive and non-reproductive females. Finally, the propharyngeal glands were most developed in the worker caste and of similar relative size in males and queens. Their function is still enigmatic.     

A pheromonal function for the crural glands of the onychophoran Cephalofovea tomahmontis (Onychophora: Peripatopsidae)

A characteristic feature of onychophorans is the presence of crural glands in males. These exocrine glands open on the ventral surface at the base of the legs. Their restriction to males suggests a sexual function. Histochemical staining of the glands indicates that their secretion has both a lipid and a protein component. Behavioural bioassays show that the secretion acts as a pheromone attractive to conspecific females. The production of a sex pheromone in onychophorans is discussed in relation to their ecology and phylogeny.     

Comparative Density of Hair Sensilla on the Legs of Cavernicolous and Epigean Harvestmen (Arachnida: Opiliones)

To allow an animal to behave appropriately, the location of sensorial structures is expected to be related to their function. As the different leg pairs of arachnids may have different functions (probing x supporting the body), one could expect them to have a different density of sensilla. Moreover, different regions of the same leg (dorsal, lateral, and ventral) would also be expected to have different densities of sensilla, according to the use of each region (e.g., the ventral part is often in contact with the substrate while the dorsal part is not). As cavernicolous animals are expected to be more sensitive than their epigean relatives, one could also expect a different density of sensilla when comparing cavernicolous and epigean animals. Using three epigean and three cavernicolous species of harvestmen (Arachnida, Opiliones), this study aimed at describing the morphology of hair sensilla on the legs and answering three questions: (1) Are there differences in the density of hair sensilla between the dorsal, lateral and ventral regions of each leg pair of the same individual? (2) Are there differences in the density of hair sensilla between the leg pairs of the same individual? (3) Are there differences in the density of hair sensilla when comparing the leg pairs of individuals of cavernicolous and non-cavernicolous species? The tarsi and metatarsi of all right legs of the six studied species were analyzed under a scanning electron microscope. The results (P < 0.05) showed that, in general: the ventral region of the tarsus was denser in sensilla trichodea than the lateral and dorsal regions, particularly on legs I and II; the density of sensilla chaetica did not differ on legs III and IV, but was greater on the dorsal region of legs I and II; the ventral part of legs I had the higher density of sensilla trichodea of the four pairs, whereas the second pair had the lower density; Holcobunus citrinus (Eupnoi) was the species with higher density of sensilla trichodea, on all legs; the cavernicolous species had a lower density of sensilla than the epigean species. The results are tentatively related to harvestmen behavior.     

Insights into the dynamics of hind leg development in honey bee (Apis mellifera L.) queen and worker larvae - A morphology/differential gene expression analysis

Phenotypic plasticity is a hallmark of the caste systems of social insects, expressed in their life history and morphological traits. These are best studied in bees. In their co-evolution with angiosperm plants, the females of corbiculate bees have acquired a specialized structure on their hind legs for collecting pollen. In the highly eusocial bees (Apini and Meliponini), this structure is however only present in workers and absent in queens. By means of histological sections and cell proliferation analysis we followed the developmental dynamics of the hind legs of queens and workers in the fourth and fifth larval instars. In parallel, we generated subtractive cDNA libraries for hind leg discs of queen and worker larvae by means of a Representational Difference Analysis (RDA). From the total of 135 unique sequences we selected 19 for RT-qPCR analysis, where six of these were confirmed as differing significantly in their expression between the two castes in the larval spinning stage. The development of complex structures such as the bees’ hind legs, requires diverse patterning mechanisms and signaling modules, as indicated by the set of differentially expressed genes related with cell adhesion and signaling pathways.     

The evolution of food-producing glands in eusocial bees (Apoidea,Hymenoptera)1

A food-producing role for cephalic exocrine glands has arisen independently in both taxa of highly eusocial bees, Apis and Meliponini. With several exceptions, there is little evidence that food is produced by glands of solitary bees or by most bees at lower levels of sociality. We suggest that this association with sociality is due to four adaptive features of these glands: (1) food from the glands allows feces from queens and larvae to have a small volume, (2) the queen's fecundity can be increased, (3) nutrient recovery via cannibalism can be facilitated, and (4) rearing of emergency replacement queens is accelerated. Acceleration of the rearing of other castes and of queens in the normal process of colony fission is not clearly an advantage ascribed to these glands. Trophic eggs produced by meliponine colony workers are analogous to the secretions from food-producing glands in Meliponini and Apis workers.     

New exocrine glands in the legionary ants of the genus Leptanilla (Hymenoptera,Formicidae, Leptanillinae)

Summary This paper reports the results of the first detailed study of the morphology of exocrine glands in two species of the ant subfamily Leptanillinae. Workers of Leptanilla escheri and L. japonica possess a large, unpaired sternal gland in the VIIth abdominal sternite, and an hypertrophied poison gland which is surrounded by a massive muscle layer. The sternal gland is absent in the queen of L. japonica, and the poison gland is highly degenerated. The queen is, however, endowed with a series of large, paired, intersegmental tergal and sternal glands, which occur between the IVth through the VIIth segments. The queen also posseses large spiracular plate glands.