Cockroach mating behaviors,sex pheromones,and abdominal glands (Dictyoptera: Blaberidae)

Two chemical signals are essential in all cockroach sexual behavioral sequences: the sex pheromone released by one partner, generally the female (for long distance attraction), and an aphrodisiac sex pheromone produced exclusively by male tergal glands (for female mounting and tergal contact or feeding behavior). Unlike the other cockroach groups, the males of the Oxyhaloinae species produce both chemical signals: the pheromone and the aphrodisiac. The occurrence of three patterns of mating behavior (A, B, and C), the production of male sex pheromones, and the existence in the male of developed sternal and tergal glands in seven related Oxyhaloinae species, make these cockroaches a useful model for studying the evolution of mating behavior patterns. The various types of mating behavior were not classified in the previous studies by Roth and Barth. In this report, they have been named type A (female in upper position), B (male in upper position), and C (male and female end to end). In type A mating, the male tergal glands, which are licked by the females, are well developed, whereas in types B and C, there is no licking of the male's tergal secretion by the females and the tergal glands are much less developed; the aphrodisiacs secreted by the tergal glands may no longer act in this case through contact chemoreception, but through an olfactory process involving volatile components. One common sex pheromone component seems to be acetoin. I suggest that the mating behavior tends from A toward B and C during the evolutionary process with a concomitant regression of the tergal glands and changes in the aphrodisiac emission levels. The mating behavioral sequences of cockroaches (Dictyoptera) and crickets (Orthoptera) show a striking degree of similarity and are probably examples of convergent evolution.     

Ultrastructure of the male accessory glands ofAllacma fusca(Insecta, Collembola)

The accessory glands ofAllacma fusca(L.) (Insecta, Collembola, Sminthuridae) consist of a series of secretory units that are arranged in parallel and open into the ejaculatory duct. Each unit is composed of microvillate cells stacked around a common cavity. Basal cells are involved in ion-control of fluids from the hemocoel to the cavity. The intermediate and apical cells, which have a laminar appearance and contain many microtubules, are involved in the structural integrity of the unit. Supporting cells ensheath the most apical cells. Large openings in the cuticle allow the gland secretion to flow into the ejaculatory duct lumen. These openings are protected by a porous cuticle different from that lining the epithelium of the ejaculatory duct. Conspicuous muscle fibers run along the lateroventral side of the ejaculatory duct beneath the insertion of the accessory glands. The fine structure of the accessory glands indicates that they are type I ectodermic glands as defined by Noirot & Quennedey (1974). Their function could be to control the fluidity of the material for spermatophore formation and to ensure the proper physiological conditions for spermatozoa stored in the ejaculatory duct lumen.     

The salivary glands of the cockroach Nauphoeta cinerea (Olivier)

The innervation of the salivary gland of the cockroach Nauphoeta cinerea (Olivier) has been investigated with the use of light and scanning electron microscopy. Light microscopy of methylene blue stained glands reveals the presence of a dual innervation arising from the ventral nerve cord and the stomodeal nervous system; the principal innervation is that from the ventral nerve cord which passes to the gland via the reservoir ducts. Branches of these nerves form a plexus on the acinar surface, the axons of which exhibit swelling at irregular intervals. The presence of this surface plexus and the axonal swellings was confirmed by scanning electron microscopy both in normal glands and in those in which the basal lamina had been removed by means of an HCl-collagenase digestion method. No acinar plexus was seen to be formed by branches of the stomatogastric nerve that were associated with the gland. However, other branches of this nerve were clearly connected with a complex network of multipolar neurones on the surfaces of the anterior regions of both salivary reservoirs.     

Morphology of the male and female tergal glands of the woodroach Cryptocercus punctulatus (Insecta,Dictyoptera)

Summary Males and females of Cryptocercus punctulatus possess tergal glands which differ in position, size, morphology, and chemical composition of their secretions. Ultrastructural studies reveal the presence of class 1 and class 3 glandular units interspersed throughout the glands; class 3 glandular units are 30 times as numerous as in the female, but no cytological difference was found between the sexes. The morphology of the tergal glands is characterized by the occurrence of a subcuticular space reservoir, a dense tracheal system, and a thick collagenous layer instead of the typical basement membrane. Comparison with the termite abdominal gland system indicates a great similarity in the fine structure. The biological function of the tergal glands is discussed.Abbreviations A Class 1 gland cell - B Class 3 gland cell - cf Collagen fibrils - d Duct - ea End-apparatus - EC Endocuticle - ef Epicuticular filaments - ep Epicuticle - j Septate junctions - m Mitochondria - mt Microtubules - mv Microvilli - pc Pore-canal - R Intracuticular reservoir - rc Receptor canal - S Saccule cell - t 6–10 Terga 6 to 10 - TG Tergal gland - tr Trachea - * Subcuticular space - Secretory material - Secretory vesicles - Pinocytosis vacuoles     

The possibility of sex and nymph discrimination by the male cockroach,Nauphoeta cinerea

The possibility of sex and nymph discrimination by males was investigated in the cockroach,Nauphoeta cinerea (Olivier). A sexually mature male takes a courting position toward a sexually mature female when he comes into contact with her and recognizes her through antennal contact. In contrast, males often behave aggressively toward each other: they bite at each others; wings and/or legs, chase each other and antennate mutually. The male, however, does not show conspicuous behavior (mating behavior or aggressive behavior) toward nearby nymphs. The male produces audible sounds when he courts a sexually mature but non-receptive female who does not respond to his courtship behavior. We found that the male also stridulates after he repeatedly courts immature teneral females, males and (last-instar) nymphs. After the bodies of teneral insects are sclerotized, the male shows courship and stridulation behavior toward sexually mature but non-receptive females but not toward mature males and nymphs. At this stage the male begins to behave aggressively toward other post-teneral mature males. We think that the variability of the sexually mature male's behavior toward other conspecifics (courtship behavior toward female, aggressive behavior toward male and no conspicuous response toward nymph) results from the male's recognition of adult and nymph.     

Morphological evidence for a probable secretory site of the male sex pheromones of Nauphoeta cinerea (blattaria,blaberidae). 2. electron microscope studies

Light and electron microscopy of the glandular epithelium of intersegmental membranes between sternites three and seven and tergites two and eight of various age groups of Nauphoeta cinerea male adults and one age group of female adults discloses differences in the epithelia of the intersternite and intertergite. The intersternal epithelium appears thicker, more glandular, and stratified. Altogether, seven cell types are recognizable, six in the male and two in the female. They are designated as types 1, 2a, 2b, 2c, 3, 4, and 5. Of these, types 1, 2a, 3, and 4 are recognizable on the sternum; types 1, 2b, and 5 on the tergum of the mature male integuments. Types 1 and 2c are found on the sternum of mature female. The cell types undergo morphological differentiation after adult emergence and show different stages of secretory activity. Type 1 are squamous cuticle-secreting cells; type 2a, 2b, and 2c are columnar-glandular and contain electron-transparent secretory vesicles of various sizes, which increase greatly in number and size in the 5-day-old adult males when the glands are most active. The vesicular size and number also differ between types 2a, 2b, and 2c cells of the same age group. The vesicles are assumed to be derived from smooth endoplasmic reticulum. The type 2 gland cells are also provided with a secretory end apparatus lined by cuticle and bordered by microvilli through which the secretion is believed to be released by exocytosis. The end apparatus leads into a cuticular ductule that opens to the surface of the cuticle as a cup-shaped receptacle, which is more conspicuous in the male intersternite. In the active gland cells, the mitochondria near the end apparatus are swollen and vacuolated. Type 3 cells are seen only on the intersternum and are believed to secrete the cuticular ductule that proceeds from the end apparatus. Type 4 cells are also recognizable only on the male intersternum and contain closely packed, electron-dense bodies, which are most numerous in mature (5-day-old) males. Type 5 cells with their dense cytoplasm are located basally in the intertergal epithelium. The functional significance of type 4 and 5 cells in the males and type 2c cells in the female is not clear. On the basis of differences in morphology, pheromone activity, and sexual behavior, it is suggested that the pheromones secreted by the intersternal and intertergal glands in the male are different, the former secreting a seducin that attracts the female to the male and the latter an “aphrodisiac” acting as a contact pheromone important in accomplishing mating.     

The influence of environmental quality on sexual selection in Nauphoeta cinerea (Dictyoptera: Blaberidae)

We examined the impact of environmental conditions on the sexpheromone and mating behavior of the cockroach, Nauphoeta cinerea.Previous research on this species has shown that female behaviorduring courtship reflects female mate choice, male behaviorcorrelates with male social status, and the male sex pheromoneis the character used by females to assess males. In the presentstudy, males and females were allowed to develop from adultemergence to sexual maturity in either a high- or low-qualityenvironment. The environment affected the quantities of sexpheromone components. We found significantly less 3-hydroxy-2-butanoneand 4-ethyl-2-methoxyphenol, but not 2-methylthiazolidine, inthe pheromone glands of males from a poor environment. Pheromonequality was also affected; the ratios involving 2-methylthiazolidinewere altered, while the ratio 3-hydroxy-2-butanone to 4-ethyl-2-methoxyphenoldid not change. Development to sexual maturity under these environmentalconditions also influenced male and female sexual behavior.Male courtship activity reflected environmental influences;males from the low-quality environment took longer to initiatecourtship and spent more time copulating with females from allenvironments. Male quality, as assessed by females, was alsoaffected by their environment. Females were slower to respondto the courtship of males from the poor environment, regardlessof the females' own rearing environments. However, females fromthe low-quality environment also took longer to respond to thecourtship, and required more courtship, regardless of the males'rearing environments. Thus, poor environments also increasefemale choosiness. However, there was only one significant interactionterm, suggesting that the environmental effects are generaland that females do not show adaptive plasticity in mate choice.Studies of sexual selection that consider the effects of variableenvironments on behavior as well as the sexually selected morphologyin other systems are likely to provide new insights into thisevolutionary process     

Peptidase inhibitors from the salivary glands of the cockroach Nauphoeta cinerea

Inhibitory activity against subtilisin, proteinase K, chymotrypsin and trypsin was detected in the salivary glands and saliva of the cockroach Nauphoeta cinerea (Blattoptera: Blaberidae). Fractionation of the salivary glands extract by affinity chromatography followed by reverse-phase HPLC yielded five subtilisin-inhibiting peptides with molecular masses ranging from 5 to 14 kDa. N-terminal sequences and subsequently full-length cDNAs of inhibitors designated NcPIa and NcPIb were obtained. The NcPIa cDNA contains 216 nucleotides and encodes a pre-peptide of 72 amino-acid residues of which 19 make up the signal peptide. The cDNA of NcPIb consists of 240 nucleotides and yields a putative secretory peptide of 80 amino-acid residues. Mature NcPIa (5906.6 Da, 53 residues) and NcPIb (6713.3 Da, 60 residues) are structurally similar (65.4% amino acid overlap) single-domain Kazal-type peptidase inhibitors. NcPIa with Arg in P1 position and typical Kazal motif VCGSD interacted stoichiometrically (1:1) with subtilisin and was slightly less active against proteinase K. NcPIb with Leu in P1 and modified Kazal motif ICGSD had similar activity on subtilisin and no on proteinase K but was active on chymotrypsin.     

Antenna contact and agonism in the male lobster cockroach, Nauphoeta cinerea

On any given day, about 35% of 80- to 85-day-old socially na?ve male (SNM) lobster cockroaches (Nauphoeta cinerea) spontaneously adopted an aggressive posture (AP) without encountering another male [spontaneous AP (SAP)]. Although SAP SNMs showed significantly higher release of the pheromone 3-hydroxy-2-butanone (3H-2B) than non-SAP SNMs, there was no significant difference in hemolymph juvenile hormone (JH) III titer. When different body parts were tested for induction of the attack behavior, the antenna was found to be the most effective. After 1 min of contact with an antenna from another SAP SNM, attack behavior was induced in 100% of SAP and 76.2% of non-SAP SNMs, and the JH III titer was significantly increased in all responders. Among the non-SAP SNMs, the JH III titer before antenna contact was significantly lower in the non-responders than in the responders, and, although the JH III increase induced by 1 min antenna contact was similar between responders and non-responders, the final JH III titer of the non-responders was significantly lower. A similar attack response, JH III titer change, and 3H-2B release were seen when the individual's own antenna was used. After 5 min of contact with an antenna from another SAP SNM, attack behavior was induced in 100% of SAP and 82% of non-SAP SNMs; in the former, 3H-2B release was similar before and after antenna contact, but the JH III titer was significantly increased after antenna contact, while, in the latter, both 3H-2B release and JH III titer were significantly increased after antenna contact. Among the non-SAP SNMs, JH III titer in the non-responders was not elevated after 5 min antenna contact, and was significantly lower than that in the responders. A pentane-washed antenna did not induce attack behavior or increase the hemolymph JH III titer, and a pentane-washed antenna coated with 3H-2B also failed to induce attack behavior. These results indicate that N. cinerea male-male agonistic interactions, to which the vertebrate challenge hypothesis can be applied, are due to contact pheromone on the antenna, resulting in the concomitant expression of attack behavior and an increase in 3H-2B release and JH III titer.     

Parasitism and decreased response to sex pheromones in malePeriplaneta americana (Dictyoptera: Blattidae)

Parasites are known to alter the behavior of their hosts, but little is known about their effects on responses to sexual stimuli. Periplaneta americanainfected with the acanthocephalan Moniliformis moniliformiswere compared to uninfected animals in their behavioral and electroantennogram responses to a synthetic P. americanapheromone component, periplanone-B, and a pheromone mimic, bornyl acetate. In a t-maze there was no significant difference between infected animals' responses to periplanone-B and a random binomial distribution; the responses of uninfected animals were significantly nonrandom. The electroan-tennogram responses of infected and uninfected animals to bornyl acetate or periplanone-B did not differ significantly, however, indicating that the alteration probably does not occur at the peripheral level but at a central nervous system level.     

The adult cervicothoracic musculature of the cockroach, Nauphoeta cinerea (Olivier)

The cervicothoracic musculature of the adult cockroach, Nauphoeta cinerea (Olivier) is described for the first time. The adult thoracic ventral intersegmental muscles are compared with those of the nymph and of the adult cockroach, Periplaneta americana (Linnaeus).     

The influence of social experience on the behavior of male cockroaches,Nauphoeta cinerea

The influence of social experience on rates of agonistic behavior was investigated in a cockroach, Nauphoeta cinerea. Social experience was manipulated by establishing three types of groups of four identically aged males: (1) ran-domly chosen, socially naive males (control); (2) males of similar status and activity level (from treatment 1); and (3) males returned to their original hierarchy after experiencing treatment 2. In the control groups, we found stable hierarchies, significant differences in the rate of agonistic behaviors exhibited among different status males, and a significant relationship between social status and level of agonism. We also compare activity levels within and among groups after males had novel social experiences. Among similar status individuals, we found less activity than when they wereintheir original groups. When males were returned to their original groups, the level of activity increased compared to the level of activity before treatment. The social status of males was unstable after these treatments. Losing tended to result in relatively more subordinate behavior, and winning in relatively more dominant behavior by a male. Within groups, the rate of agonism also increased over 5 days in groups of males that had no previous interactions with each other, while the rate of agonism remained the same in groups of familiar males. We interpret these results in light of male-male assessment and the maintenance of social status in this species.     

Regulation of sex pheromone production in the male Nauphoeta cinerea cockroach: Role of brain extracts,corpora allata�(CA), and juvenile hormone (JH)

The neuroendocrine mechanisms underlying pheromone regulation in cockroaches are unclear because of a lack of physiological and chemical data. The present report describes experiments designed to determine the role of the brain, corpora allata, and juvenile hormone III in the production of sex pheromone by male Nauphoeta cinerea cockroaches. The levels of two sex pheromone components, i.e., acetoin and 2‐methylthiazolidine, were measured by gas chromatographic analysis of sternal gland extracts obtained from individual males. Allatectomy or decapitation performed up to 2 to 3 days after imaginal molt caused a decrease in sex phermone levels. Conversely decapitation or allatectomy performed after 3 to 4 days post‐eclosion had almost no effect on sex pheromone levels. Injection of JHIII into allatectomized and decapitated males stimulated pheromone production while injection of brain extract had no effect. These results indicate that JHIII is involved in the differentiation of sternal glands and that regulation via pheromone biosynthesis activating neuropeptide (PBAN) does not occur in N. Cinerea cockroaches. Arch. Insect Biochem. Physiol. 40:165–172, 1999. © 1999 Wiley‐Liss, Inc.     

Pheromone, juvenile hormone, and social status in the male lobster cockroach Nauphoeta cinerea

In this study, the major pheromone component, 3‐hydroxy‐2‐butanone (3H‐2B), released by dominants was measured during early scotophase. Both the JH III titer in the hemolymph and the 3H‐2B content of the sternal glands of the dominants and subordinates were then measured during late scotophase and late photophase. These investigations were performed on encounter days 1, 2, 3, 5, 7, 9, 12, and 20. The results showed that, for non‐aggressive posture (AP)‐adopting socially naïve males (SNMs), both the 3H‐2B release and the hemolymph JH III titer were maintained at a low level. Once a fight occurred, 3H‐2B release was raised significantly in the AP‐adopting dominants, but not in non‐AP‐adopting subordinates, and remained raised throughout the entire experimental period. At 30 min after the first encounter, the hemolymph JH III titer was significantly increased in dominants, but not in subordinates. A significantly higher hemolymph JH III titer was observed in dominants during late scotophase on days 3, 5, 12, and 20 and during late photophase on days 3, 5, and 20. After fighting, the sternal gland 3H‐2B content of the dominants or subordinates was significantly lower than in SNMs. In dominants, the sternal gland 3H‐2B content during late scotophase was significantly lower than that during late photophase in the first 9 domination days, while, in the subordinates, the 3H‐2B content during late scotophase was either similar to, or significantly higher than, that in late photophase. In the dominants, 3H‐2B release and JH III titer were positively correlated. In rank switchers, the switched social status was positively correlated with both 3H‐2B release and JH III titer. Comparison of 3H‐2B release and JH III titer in 1‐time, 3‐time, or 5‐time dominants showed that, although winning significantly increased both 3H‐2B release and JH III titer, there is no significant difference in 3H‐2B release between 3‐ and 5‐time winners, while the JH III titer was most significantly increased in the 3‐time winners. The possible relationship between pheromone release, JH III titer, and social status is discussed. Arch. Insect Biochem. Physiol. 2008. © 2008 Wiley‐Liss, Inc.     

Ultrastructure of male sex pheromone glands in abdominal tergites of five Lutzomyia sandfly species (Diptera: Psychodidae)

The fine structure of male sex pheromone disseminating structures on abdominal segments of five species of Lutzomyia sandflies (Diptera: Psychodidae) was analyzed. Scanning electron microscopy showed that in Lutzomyia cruzi [Mem. Inst. Oswaldo Cruz 33 (1938) 349] and Lutzomyia longipalpis [Mem. Inst. Oswaldo Cruz 4 (1912) 84], the disseminating structures are located in pale spots on abdominal tergites IV or III and IV and are morphologically similar, appearing as small round cuticular elevations with a central pore. Observation of abdominal tergites of L. longipalpis pupae showed that the spots, but not the structures, are already present in this stage. In Lutzomyia lenti [Mem. Inst. Oswaldo Cruz 33 (1938) 349] and Lutzomyia carmelinoi [Mem. Inst. Oswaldo Cruz 81 (1986) 323] adult males, the disseminating structures are present on tergal segments V and VI, where pale spots could not be observed, and appear as apple-like elevations with a central pore. In Lutzomyia renei, a single disseminating structure is found at the anterior region of tergal segment VI. Transmission electron microscopy was used to analyze the gland cell fine structure in L. cruzi. Several class III gland cells are located side by side in the fourth abdominal segment. Each epidermal secretory cell contains a small reservoir and a short outlet channel through the cuticle.     

New cockroaches from the Upper Carboniferous of Siberia (Insecta: Dictyoptera,Mylacridina)

Cockroaches (Dictyoptera, Mylacridina) from the Chunya locality (Upper Carboniferous of the Central Siberian Plateau) are considered. New representatives of the family Phyloblattidae Schneider, 1983 (Phyloblatta majuscula sp. nov., P. chunyensis sp. nov., Hesperoblatta vishniakovae sp. nov., and H. secunda sp. nov.) are described.