Knockdown of the juvenile hormone receptor gene inhibits soldier-specific morphogenesis in the damp-wood termite Zootermopsis nevadensis (Isoptera: Archotermopsidae)

The Methoprene-tolerant (Met) protein has been established as a juvenile hormone (JH) receptor. Knockdown of the Met gene caused precocious metamorphosis and suppression of ovarian development. However, the function of Met in caste development of social insects is unclear. In termites, JH acts as a central factor for caste development, especially for soldier differentiation, which involves two molts from workers via a presoldier stage. Increased JH titer in workers is needed for the presoldier molt, and the high JH titer is maintained throughout the presoldier period. Although presoldiers have the fundamental morphological features of soldiers, the nature of the cuticle is completely different from that of soldiers. We expected that JH signals via Met are involved in soldier-specific morphogenesis of the head and mandibles during soldier differentiation, especially in the presoldier period, in natural conditions. To test this hypothesis, we focused on soldier differentiation in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Met homolog (ZnMet) expression in heads increased just after the presoldier molt. This high expression was reduced by ZnMet double stranded (dsRNA) injection before the presoldier molt. Although this treatment did not cause any morphological changes in presoldiers, it caused strong effects on soldiers, their mandibles being significantly shorter and head capsules smaller than those of control soldiers. Injection of ZnMet dsRNA throughout the presoldier stage did not affect the formation of soldier morphology, including cuticle formation. These results suggested that the rapid increase in ZnMet expression and subsequent activation of JH signaling just after the presoldier molt are needed for the formation of soldier-specific weapons. Therefore, besides its established role in insect metamorphosis, the JH receptor signaling also underlies soldier development in termites.     

Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae

Termites exploit microbially rich resources such as decayed wood and soil that are colonized by potentially pathogenic and parasitic fungi, bacteria, viruses, and nematodes. In colonies composed of thousands of individuals, the risk of infection among nestmates is significant, and individual and social behavior could involve various adaptations to resist disease and parasitism. Here we show that the dampwood termite Zootermopsis angusticollis (Hagen) exhibits a dosage dependent susceptibility to the soil nematode Steinernema carpocapsae (Weiser) (Mexican strain) and that this social insect significantly alters its behavior in response to this entomopathogenic roundworm. Relative to their baseline behavior, termites exposed to infective juveniles increased the frequency and duration of allogrooming and vibratory displays as well as two other novel behaviors, abdominal tip-raising and self-scratching. Whereas the first two behaviors likely reflect general adaptations to reduce susceptibility to a variety of pathogens and parasites, the latter behaviors might be specific to nematodes because they have never been observed in Z. angusticollis in any other pathogenic context. Our results support the hypotheses that behavioral responses in termites are important in the control of pathogenic and parasitic microorganisms and that termite susceptibility is socially mediated.     

Cyclic carbon dioxide release in the dampwood termite, Zootermopsis nevadensis (Hagen)

Real-time traces of CO(2) release of pseudergates of the dampwood termite, Zootermopsis nevadensis (Hagen) were obtained using flow-through respirometry. Traces were made at each of six temperatures, between 10 and 35 degrees C. Termites released CO(2) in a cyclic pattern at each of the six temperatures. CO(2) release rate (as V(CO(2)) in ml h(-1)) increased significantly with temperature and body mass. Rate of change in V(CO(2)) with temperature (or Q(10)) was 2.11. Degree of cycling in CO(2) traces was estimable using the coefficient of variability. Coefficient of variability for both acyclic and cyclic traces declined exponentially with increasing temperature.     

Morphology and gonad development of normal soldiers and reproductive soldiers of the termite Zootermopsis nevadensis nevadensis (Isoptera, Archotermopsidae)

Reproductive or neotenic soldiers of the Archotermopsid Zootermopsis nevadensisnevadensis (Hagen) are compared to sterile soldiers and primary male reproductives. Several head capsule morphometrics correlate significantly with gonad size across all forms and both sexes of soldiers. The easily observed field character of ratio of mandible length to labrum length is a consistent and reliable feature of head capsule external morphology for predicting gonad development and reproductive potential of soldier forms regardless of age, sex, or live weight.     

Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis

Abstract.  Termite primary reproductives may be exposed to pathogens when dispersing from their parental nest and establishing a new colony. Immunity and reproduction are investigated during colony foundation by implanting a nylon filament into the abdomen of mated and unmated female and male primary reproductives of the dampwood termite Zootermopsis angusticollis. Primary reproductives are paired in combinations of female/male, female/female and male/male and, using confocal microscopy, immune defence is assessed by measuring the degree of encapsulation of nylon implants during three periods of colony foundation: (I) shortly after pairing; (II) during copulation/oocyte maturation; and (III) during oviposition. There are differences in the encapsulation response of mated and unmated termites that are contingent on the period of colony foundation when termites are challenged. Mated females and males have significantly greater encapsulation responses than their unmated counterparts shortly after pairing, perhaps as a prophylactic measure against exposure to disease. The encapsulation response of mated and unmated males does not differ significantly during periods II and III. The onset of oviposition is significantly delayed in mated females that received implants during periods I and II. Mated females have a significantly reduced encapsulation response during the time of copulation and oocyte maturation, but not during oviposition. Overall, males have a significantly greater ability than females to encapsulate a nylon implant. The findings suggest that reproduction can reduce the immune response in female primary reproductives. The results are discussed in light of trade-offs between immunity and reproduction during the critical life-history phase of colony establishment in termites.     

Influence of sex-specific stimuli on ovarian maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis

Abstract. It was hypothesized that female primary and secondary reproductives of the termite Zootermopsis angusticollis Hagen require sex-specific stimuli from a reproductive male to trigger ovarian maturation. To test this hypothesis, experimental laboratory colonies were established that contained female primary or secondary reproductives nesting: alone; with a male; with a female; and with three third- to fourth-instar larvae. Following colony initiation, we measured changes in body mass, ovariole number and fecundity over 60 days. Results indicate that the reproductive maturation of female primaries was promoted by contact with a male but inhibited by the presence of another female. Secondary females were not affected by the presence of another reproductive, regardless of sex, but the development of reproductive competency of primary females appeared to depend on male-specific stimulation. Reliance on male–female interaction to induce female reproductive development may ensure that the resources of newly dealate females are not wasted on producing larvae that would have a poor chance of surviving in the absence of a male. By contrast, secondary females maturing within established colonies are likely to have a mate and immediate assistance with non-reproductive tasks, and therefore do not delay ovarian maturation and reproduction until they perceive male-specific stimuli. These results demonstrate that male-specific stimuli affect only the reproductive development of primary females, and suggest that the degree to which primary and secondary females depend on mate assistance may have shaped their physiological responses to the presence of a reproductive male.     

Social influence of larvae on ovarian maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis

We tested the effect of larvae on the reproductive maturation and fecundity of female primary and secondary reproductives of the termite Zootermopsis angusticollis Hagen (Isoptera; Termopsidae) by varying the number of third‐ to fourth‐instar larvae nesting with heterosexually paired reproductives. Primary females had higher fecundities and oviposited sooner when nesting with larvae than females lacking larvae, but gained less body mass and had fewer functional ovarioles per ovary. Secondary reproductives nesting with larvae also had higher fecundities and oviposited sooner, but unlike primaries, they gained more body mass and had more functional ovarioles when larvae were present. The specific response of both primary and secondary females varied according to the number of larvae present. These results suggest that larvae can enhance the fecundity of primary and secondary females. Larvae may increase the energetic reserves of reproductives by performing colony labour, reducing pathogen load and providing trophallactic secretions. Trophallaxis with larvae may significantly enhance endogenous nitrogen, which is a limiting nutrient for termites. Primary females, which normally need to produce a first brood quickly to initiate a new colony, may expend limited nutritional resources on oogenesis rather than producing additional ovarioles. Primaries may also store fewer energetic reserves for long‐term brood care, and therefore gained less mass when larvae were present to attend to non‐reproductive tasks. Secondary females may exhibit a greater positive response to larvae than primaries because they begin reproductive life with fewer stored resources and thus their development and fecundity are more dependent on assistance from larvae. Both primary and secondary reproductives may become more dependent on the contributions of larvae as their rate of egg production increases with subsequent bouts of oviposition.     

The influence of group size on ovarian development in adult and neotenic reproductives of the termite Zootermopsis angusticollis (Hagen) (Hodotermitidae)

Termite imagines of Zootermopsis angusticollis (Hagen), while still in the colony as winged individuals, do not show ovary development, although vitellogenin is present in the blood at low levels. When removed from the colony, artificially dealated, and paired, vitellogenin levels rise: subsequently ovaries develop resulting in oviposition approximately 15–16 days after removal from the colony. Imagines removed from the colony, dealated and held together in a heterosexual group, however, show little or no ovary development after 25 days, although vitellogenin is present in the haemolymph in low levels. Newly developed neotenic reproductives, on the other hand, removed from the colonly 1–2 days after the neotenic moult, and isolated in heterosexual pairs for 60 days, had ovaries which did not become larger than 0.02 mm³, and no eggs were laid. This is in contrast to the normal ovary development of neotenic reproductives produced in groups of larvae, as described earlier. Vitellogenin levels in isolated pairs of neotenics were low until 25 days after isolation, while vitellogenin levels increased 7–9 days after the moult in female neotenics kept in a colony with larvae. The results of this study on ovarian development and vitellogenesis in neotenic and adult reproductives reflect the normal biology of the two reproductive types where the latter leave the colony to found new colonies, while neotenics become sexually mature within the colony in which they developed.     

Disease and colony establishment in the dampwood termite Zootermopsis angusticollis: survival and fitness consequences of infection in primary reproductives

Pathogens have likely infl uenced life-history evolution in social insects because their nesting ecology and sociality can exacerbate the risk of disease transmission and place demands on the immune system that ultimately can impact colony survival and growth. The costs of the maintenance and induction of immune function may be particularly significant in termites, which have a nitrogen-poor diet. We examined the effect of fungal exposure on survival and reproduction during colony foundation in the dampwood termite Zootermopsis angusticollis by experimentally pairing male and female primary reproductives and exposing them to single (‘acute’) and multiple (‘serial’) dosages of conidia of the fungus Metarhizium anisopliae and recording their survival and fitness over a 560 day period. The number of eggs laid 70 days post-pairing was significantly reduced relative to controls in the serial-exposure but not the acute-exposure treatment. Reproduction thus appeared to be more resilient to a single pathogen exposure than to serial challenge to the immune system. The impact of fungal exposure was transient: all surviving colonies had similar reproductive output after 300 days post-pairing. Our results suggest that disease can have significant survival and fitness costs during the critical phase of colony foundation but that infection at this time may not necessarily impact long-term colony growth. Received 25 February 2005; revised 27 September and 20 October 2005; accepted 20 December 2005.     

Cyclic carbon dioxide release in the dampwood termite, Zootermopsis nevadensis (Hagen)

Real-time traces of CO₂ release of pseudergates of the dampwood termite, Zootermopsis nevadensis (Hagen) were obtained using flow-through respirometry. Traces were made at each of six temperatures, between 10 and 35°C. Termites released CO₂ in a cyclic pattern at each of the six temperatures. CO₂ release rate (as in ml h⁻¹) increased significantly with temperature and body mass. Rate of change in with temperature (or Q₁₀) was 2.11. Degree of cycling in CO₂ traces was estimable using the coefficient of variability. Coefficient of variability for both acyclic and cyclic traces declined exponentially with increasing temperature.     

Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae)

Sexual communication can contribute to population divergence and speciation because of its effect on assortative mating. We examined the role of communication in assortative mating in the Enchenopa binotata species complex of treehoppers. These plant-feeding insects are a well studied case of sympatric speciation resulting from shifts to novel host-plant species. Shifting to hosts with different phenologies causes changes in life-history timing. In concert with high host fidelity, these changes reduce gene flow between populations on ancestral and novel hosts and facilitate a rapid response to divergent natural selection. However, some interbreeding can still occur because of partial overlap of mating periods. Additional behavioral mechanisms resulting in reproductive isolation may thus be important for divergence. In E. binotata, mating pairs form after an exchange of plant-borne vibrational signals. We used playback experiments to examine the relevance of inter- and intraspecific variation in male advertisement signals for female mate choice in a member of the E. binotata species complex. Female signals given in response to male signals provided a simple and reliable assay. Male species and male individual identity were important determinants of female responses. Females failed to respond to the signals of the two most closely related species in the complex, but they responded strongly to the signals of conspecific males, as well as to those of the most basal species in the complex. Communication systems in the E. binotata species complex can therefore play a role in reproductive isolation. Female responses were influenced by among-individual variation in male signals and females, suggesting the involvement of sexual selection in the evolution of these communication systems.     

Foraging vibration signals attract foragers and identify food size in the drywood termite, <Emphasis Type="Italic">Cryptotermes secundus</Emphasis>

Information gathering and communication behaviour has evolved within constraints of size, physiology and ecology of the animal. Due to these constraints, small herbivorous insects are likely to use substrate borne vibrations for information gathering and communication. Although such signals have been characterised in many types of insects, including group-living insects, they are poorly known in termites.We showed that the Australian drywood termite Cryptotermes secundus could determine the size of wooden blocks by using the vibrations generated during foraging. The termites behaved differently in choice experiments when artificially generated vibration signals were played compared with natural recordings, indicating that these termites can discriminate the source of the vibration as well. AT-maze experiment showed that the termites were attracted to the natural recordings of feeding termites, suggesting that vibrations are important in communication during foraging as well as food resource assessment. Combining the effects of food size preference and attraction to other termites explained differences in behaviour between artificially generated vibration signals compared with natural recordings. This study demonstrates that termites use substrate borne vibrations for information gathering and communication as predicted. Received 21 March 2007; revised 19 June and 7 August 2007; accepted 20 August 2007.     

Vibrational communication during spawning behavior in the himé salmon (landlocked red salmon,Oncorhynchus nerka)

Summary Sexual behaviors of the salmon are composed of a stimulus-reaction chain, which ensures synchronous spawning between the sexes and successful fertilization. To characterize the signals involved in such a stimulusreaction chain, the body vibration and electromyographic activity of the trunk muscles during spawning were simultaneously recorded from freely behaving male and female pairs of himé salmon (landlocked red salmon,Oncorhynchus nerkd) and were analyzed in combination with a videographic analysis of behavior sequences. The results showed that the himé salmon have an elaborate communication system in which characteristic vibrational signals are exchanged. These are produced by body vibration due to trunk muscle activity related to spawning and are transmitted between the sexes with an accurate timing through the stimulus-reaction chain. They act as timing cues to synchronize gamete release and are thought to be shared among a wide variety of fishes. It was hypothesized that the lateral line sense is involved in the detection of these vibrational signals. Furthermore, based on the sequence matrix analysis as well as on information theory, intersexual behavioral sequences during spawning were analyzed statistically. The results showed that statistically significant interactions occur between the sexes and statistically significant amounts of information are transmitted through the interactions, supporting the results from recording experiments mentioned above. Characters of the signalling system and possible origins of the vibrational signals are also discussed.     

Vertical stratification of the termite assemblage in a neotropical rainforest

The importance of termites as decomposers in tropical forests has long been recognized. Studies on the richness and diversity of termite species and their ecological function have flourished in more recent times, but these have been mostly conducted in a thin stratum within a standing man’s reach. Our aims were to evaluate the specific richness and composition of the termite assemblage in the canopy of a tropical rainforest and to determine its originality with respect to the sympatric ground-level fauna. We conducted systematic searches for canopy termites, together with conventional sampling of the sympatric ground-level fauna, in the San Lorenzo forest, Panama. We hypothesized that (1) the canopy accommodates two categories of wood-feeding termites (long-distance foragers and small-colony “one-piece” species) and possibly soil-feeders in suspended soil-like habitats; (2) due to the abundance of soil-feeders, the overall diversity of the ground fauna is higher than that of the canopy; (3) differences in microclimate and resource accessibility favour vertical stratification among wood-feeders. Sixty-three canopy samples yielded ten species of termites, all wood-feeders. Five of these were not found at ground level, although a total of 243 ground samples were collected, representing 29 species. In addition to long-distance foragers (Microcerotermes and Nasutitermes spp.) and small-colony termites (mostly Kalotermitidae), the canopy fauna included Termes hispaniolae, a wood-feeding Termitidae from an allegedly soil-feeding genus, living in large dead branches. Soil-feeders were absent from the canopy, probably because large epiphytes were scarce. As predicted, the ground fauna was much richer than that of the canopy, but the species richness of both habitats was similar when only wood-feeders were considered. Vertical stratification was strongly marked among wood-feeders, as all common species, apart from the arboreal-nesting Microcerotermes arboreus, could unequivocally be assigned to either a ground or a canopy group. The canopy, therefore, contributes significantly to the total species richness of the termite assemblage, and the diversity, abundance and ecological importance of canopy termites in tropical rainforests may be higher than previously recognized.Electronic Supplementary Material Supplementary material is available to authorized users in the online version of this article at .     

The influence of the vibration signal on worker interactions with the nest and nest mates in established and newly founded colonies of the honey bee, Apis mellifera

Honey bees adjust cooperative activities to colony needs, based in part on information acquired through interactions with the nest and nest mates. We examined the role of the vibration signal in these interactions by investigating the influence of the signal on the movement rates, cell inspection activity, and trophallaxis behavior of workers in established and newly founded colonies of the honey bee, Apis mellifera. Compared to non-vibrated control bees, vibrated recipients in both colony types exhibited increased movement through the nest and greater cell inspection activity, which potentially increased contact with stimuli that enhanced task performance. Also, compared to controls, recipients in both colony types showed increased rates of trophallactic interactions and spent more time engaged in trophallaxis, which potentially further increased the acquisition of information about colony needs. The vibration signal may therefore help to organize labor in honey bees in part by increasing the rate at which workers obtain information about their colony. Vibrated recipients in the established and newly founded colonies did not differ in any aspect of behavior examined, suggesting that colony developmental state did not influence the degree to which individual workers responded to the signal. However, previous work has demonstrated that newly founded colonies have increased levels of vibration signal behavior. Thus, the vibration signal may help to adjust worker activity to colony conditions partly by stimulating greater numbers of bees to acquire information about colony needs, rather than by altering the level at which individual recipients react to the signal. Received 23 October 2006; revised 15 January 2007; accepted 7 February 2007.     

萤火虫(鞘翅目:萤科)两性交流中的闪光信号

对国内外萤火虫两性交流闪光信号的研究进行了综述,萤火虫发光器因种而异,多数发出黄绿色萤光,闪光信号的频率、光谱、强度及其时空分布的闪光模式包含着两性交流信息。萤火虫闪光交流系统有两种分类方法,其一是萤火虫具两个类型的闪光信号交流系统,及系统和系统,前者多在旧大陆,后者多在新大陆;其二是萤火虫具6个类型闪光信号交流系统,即HP,LL,LC,PR,CR和LB型,其中PR型与系统相对应,HP型与系统对应。萤火虫两性交流闪光信号常因时间和空间上的差异及外界物体的干扰使两性闪光交流的效率受到影响。萤火虫两性交流的闪光信号起源于鞘翅目的幼虫阶段,并起警戒天敌的作用,经过两性选择成为成虫两性交流的一种途径,进而成为新大陆的一些萤火虫间捕食猎物和逃避天敌的生存策略。     

Sex pheromones and trail‐following pheromone in the basal termites Zootermopsis nevadensis (Hagen) and Z. angusticollis (Hagen) (Isoptera: Termopsidae: Termopsinae)

In the context of an evolutionary study of the chemical communication in termites, sex pheromones and trail‐following pheromones were investigated in two Termopsidae, Zootermopsis nevadensis and Z. angusticollis. In these species, in which the presence of sex‐specific pheromones has been demonstrated previously, the chemical structure of the female sex pheromone has now been identified as (5E)‐2,6,10‐trimethylundeca‐5,9‐dienal and the male sex pheromone as (+)‐ or (?)‐syn‐4,6‐dimethyldodecanal. The amount of sex pheromone was estimated at 5–10 ng per individual in females and 2–5 ng in males. Because these two sympatric species do not differ in their pheromonal chemical composition, reproductive isolation is probably mediated chiefly by differences in dispersal flight chronology. The trail‐following pheromone was shown to be composed of the same compound as the male sex pheromone, that is syn‐4,6‐dimethyldodecanal. The compound syn‐4,6‐dimethyldodecanal was 10 times more active than the racemic (+/?)‐syn + (+/?)‐anti‐4,6‐dimethyldodecanal in eliciting trail‐following. The amount of syn‐4,6‐dimethyldodecanal was estimated at 0.1–0.5 ng per pseudergate. Regarding the phylogenetic aspects, the nature of the female sex pheromone of Zootermopsis is structurally akin to the trail‐following pheromone of Mastotermes darwiniensis of Mastotermitidae and Porotermes adamsoni and Stolotermes victoriensis of Termopsidae. Interestingly, the nature of the trail‐following pheromone of the Termopsinae Zootermopsis is clearly different from that of the Porotermitinae P. adamsoni and the Stolotermitinae S. victoriensis, which mirrors recent molecular data on the paraphyly of Termopsidae. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 519–530.