Biparental care in incipient colonies of the dampwood termiteZootermopsis angusticollis Hagen (Isoptera: Termopsidae)

Parental care and division of labor in male and female primary reproductives in incipient colonies of the dampwood termite Zootermopsis angusticolliswere studied by recording repertory sizes, behavior frequencies, time budgets, and transition probabilities of acts. Repertory sizes for males and females were identical, and behaviors were performed at similar frequencies. Time budget data also suggested equal participation in parental care by both sexes. Transition probability analysis suggested that males and females did not organize their behavior in roles. We therefore found no indication of sex-based division of labor during colony foundation and the incipient stages of colony growth. The lack of behavioral specialization may be due to the fact that acts might be related and/or have more than one function, and different tasks are not spatially associated. Our observations are consistent with the hypothesis that monogamous mating systems in termites involve mate assistance.     

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.     

Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites,Zootermopsis (Isoptera: Termopsidae)

The dampwood termite genus ZootermopsisEmerson contains three recognized species with four distinct and consistent hydrocarbon phenotypes. Agonistic behaviors among nonreproductive insects from colonies of the same and different hydrocarbon phenotypes were observed in the laboratory. Various combinations of soldier versus nymphs, pseudergate versus pseudergate, and soldier versus soldier encounters were used in experimental trials. Soldiers or pseudergates seldom attack individuals of the same hydrocarbon phenotype. Z. angusticollis(Hagen) (phenotype II) is typically aggressive toward phenotype III of Z. nevadensis(Hagen) but not always aggressive against phenotype I of Z. nevadensis.The variation in response is dependent on which castes are placed in the bioassay arena: soldier versus soldier bouts result in consistent aggression, while pseudergate versus pseudergate or soldier versus nymphs contacts do not. Both pseudergates and soldiers of Z. laticeps(Banks) (phenotype IV) respond agonistically toward the other three phenotypes: Z. angusticollis (II) and Z. nevadensis(I and III). Although hydrocarbon phenotypes I and III, both Z. nevadensis,are morphologically indistinguishable, agonistic behavioral responses between phenotype I and phenotype III are not equivalent to I versus I or III versus III behavioral responses. The I versus III engagements, regardless of the castes involved, display a greater proportion of avoidance and aggressive responses than I or III intraphenotype encounters. We interpret the lack of avoidance or aggressive behavior within each of the two phenotypes of Z. nevadensisand the significant avoidance and aggressive behavior between phenotypes as definite evidence of discrimination between disparate hydrocarbon phenotypes. These agonistic bioassays along with data on distinct hydrocarbon patterns and geographic distributions serve as the basis for creating two subspecies of Z. nevadensis: Z. n. nevadensis(Hagen) and Z. n. nuttingiHaverty and Thorne, ssp. nov.     

Microsatellite markers for two species of dampwood termites in the genus Zootermopsis (Isoptera: Termopsidae)

Dampwood termites in the genus Zootermopsis inhabit forested areas in western North America. To better understand the colony composition and breeding structure of Zootermopsis, we identified polymorphic microsatellite loci to use in population analysis. Microsatellite loci were isolated from Zootermopsis nevadensis nevadensis (Hagen); however, all primers amplified homologous loci in Zootermopsis angusticollis (Hagen) and Zootermopsis nevadensis nuttingi (Hagen). Twelve loci were polymorphic in one or more of the above subspecies and species. The number of alleles per locus ranged from one to six, with some allelic differences among subspecies and species. We are currently utilizing the microsatellite markers to investigate the population genetics of Zootermopsis.     

圆唇散白蚁补充生殖蚁的类型与建群能力

摘要: 【目的】为了探讨圆唇散白蚁Reticulitermes labralis补充生殖蚁对巢群稳定和发展的作用。【方法】对野外巢群进行调查研究, 及对婚飞成虫通过雌雄配对与补充生殖蚁隔离巢群进行人工饲养的对比研究。【结果】在野外巢群只发现1对原始蚁王蚁后, 而补充生殖蚁的数量最多可达到689头/巢。圆唇散白蚁有3种类型的补充生殖蚁, 即由工蚁转化来的无翅型补充生殖蚁、若蚁转化来的翅芽型补充生殖蚁和末龄若蚁羽化来的拟成虫型补充生殖蚁。实验室条件下婚飞配对群体和隔离群体建群1个月后的存活率分别为64%和96%。建巢初期婚飞配对群体的子代数目增长缓慢, 2个月时的群体数量为6.3±1.54, 10个月时的群体数量也仅为8.4±1.47; 而隔离建群补充生殖蚁2个月时的群体数量为52.4±6.44, 10个月时的群体数量为164.3±20.85, 都高于婚飞配对群体。 此外, 野外巢群的补充蚁后跟原始蚁后一样都具有发达的卵巢。【结论】在圆唇散白蚁中补充生殖蚁是白蚁巢群主要的繁殖力量, 也是建立新巢群的重要繁殖品级。     

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.     

Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae)

In termites, a male and a female usually found a colony cooperatively. However, pairing efficiency tends to be low in Reticulitermes speratus because of a limited mate-searching range, the female-biased sex ratio, and a relatively low calling ability. Females that fail to pair with males found colonies either in female–female pairs or even alone. In the laboratory, we examined colony foundation by single females (F), female–female pairs (FF), and normal male–female pairs (FM). The time until colony foundation (when termites began excavating wood baits) differed significantly among the unit types. Time until excavation was much longer for single females than for FF and FM units, which reflects the relative success of colony foundation. The survival rate of single females was also significantly lower than that of FF- and FM-unit females, although there was no difference between FF and FM units. This result demonstrates that cooperation, even female–female, promotes female survivorship. Nevertheless, the number of progeny per female was significantly lower in FF units than in FM units, possibly because females of FF units must share reproductive output. These results lead us to the conclusion that a normal monogamous pair is the best unit for colony foundation. Nevertheless, females alone can establish colonies by parthenogenesis, and even female–female cooperation promotes colony foundation success if pairing with males is not possible. Considering the functional decision for females in F and FF units of how much time to spend searching for a male mate, we believe that these facultative pathways of colony foundation by parthenogenesis have adaptive significance. Received: November 30, 2000 / Accepted: March 6, 2001     

黑翅土白蚁巢群觅食群体大小与工蚁体长呈正相关

【目的】明确黑翅土白蚁Odontotermes formosanus巢群的觅食群体大小与工蚁体长之间的关系,为进一步研究其生态学特点以及更好地开展防治提供依据。【方法】在杭州植物园内选择5处有黑翅土白蚁活动区域作试验点,诱捕并以中性红(neutral red)标记捕获的白蚁工蚁,通过“捕获-标记-释放-重捕”试验测定黑翅土白蚁的觅食群体大小。【结果】5个试验点中有4个成功实施了“捕获-标记-释放-重捕”试验,4个试验点黑翅土白蚁巢群的觅食群体个体数量分别为443 133±45 469, 495 360±67 429, 674 345±101 703和1 224 662±93 112头。黑翅土白蚁觅食群体大小(Y)与觅食工蚁的体长(X)呈正相关,拟合的指数函数方程式为：Y=1.8389e^0.7185X(R²=0.7834)。【结论】本研究明确了黑翅土白蚁的觅食群体大小以及工蚁体长之间的函数关系,为开展区域防治提供了依据。     

Comparative study of incipient colony development in the Formosan subterranean termite, <Emphasis Type="Italic">Coptotermes formosanus</Emphasis> Shiraki (Isoptera,Rhinotermitidae)

Summary The Formosan subterranean termite, Coptotermes formosanus Shiraki is the most destructive, difficult to control and economically important species of termite in the southern United States. At present, no information is available on the genetic relatedness of primary Formosan subterranean termite reproductives that establish new colonies. Information on survivorship and fitness components of primary reproductives from different sibships (sibling or nonsibling) is helpful to our understanding of biological and ecological characteristics of different breeding generations in C. formosanus. The present study examined the effects of sibship and colony origin on growth and mortality of incipient colonies of C. formosanus. Seven stock colonies of C. formosanus were collected in 1996 through 1997 in New Orleans and Lake Charles, La, USA. A total of 338 incipient colonies of sibling pairs or nonsibling pairs of C. formosanus were set up. The study indicated that mate relatedness significantly affected mortality and fitness. Nonsibling mates suffered significantly higher mortality than sibling mates originated from New Orleans. However, the decreased success of outbred mates was offset by an increased fecundity compared to inbred colonies over time. Both sibling- and nonsibling-founded colonies from Lake Charles had a significantly higher survival rate than did colonies from New Orleans. Colonies from Lake Charles also produced a significantly higher number of larvae/workers than colonies from New Orleans. The mismatch of habits by mates from different locations and the potential for greater disease risks may be associated with higher mortality in outbred pairs. However, heterozygous offspring of outbred pairs probably have increased genetic variation, which provides greater adaptation potential, thus making the colony more robust in the face of environmental fluctuations.Received 11 March 2002; revised 26 February 2003; accepted 14 March 2003.     

Chemical and molecular identification of the invasive termite <Emphasis Type="Italic">Zootermopsis nevadensis</Emphasis> (Isoptera: Archotermopsidae) in Japan

Numerous termite species have been introduced outside their native ranges by human transport, and some have become invasive. The dampwood termite Zootermopsis nevadensis (Hagen), which is native to western North America, has been introduced to and become established in Kawanishi City, Hyogo Prefecture, Japan. Zootermopsis nevadensis is subdivided into two subspecies based on cuticular hydrocarbon (CHC) phenotypes: Z. nevadensis nevadensis and Z. nevadensis nuttingi (Haverty and Thorne). Here, we identified Z. nevadensis in Japan as hybrids between the two subspecies. Chemical analysis showed the presence of 7,15-dimethylhenicosane and 5,17-dimethylhenicosane in the CHCs of Z. nevadensis in Japan, corresponding to the CHC phenotype of Z. n. nevadensis. Conversely, all mitochondrial cytochrome c oxidase subunit I sequences of Z. nevadensis in Japan were identical to sequences from Z. n. nuttingi and hybrids between the two subspecies from a native hybrid zone in California, USA. In addition, phylogenetic analysis showed that Z. nevadensis in Japan formed a clade with Z. n. nuttingi and hybrids between the two subspecies. Our results show discordance between the chemical and genetic features of Z. nevadensis in Japan, indicating that individuals of Z. nevadensis in Japan are hybrids between the two subspecies.     

Seasonal patterns of egg production in field colonies of the termite <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera: Rhinotermitidae)

This is the first report on the annual egg production patterns in mature termite colonies in the field. Data on the seasonal patterns of egg production in field colonies are very important for understanding the annual colony growth schedule, resource allocation, and population dynamics of the termites. However, collecting the eggs from a sufficient number of colonies is extremely difficult in Reticulitermes termites because their multiple-site nesting makes it difficult to find the reproductive center of the colonies. Here, we first show the seasonal pattern of egg production in the subterranean termite Reticulitermes speratus by collecting the reproductive center of ten colonies each month from April through October. We had to destructively examine dozens of nests to find eggs from enough field colonies each month. Mature field colonies began to produce eggs in late May, soon after the swarming season, and the egg production rate (EPR) reached its maximum in early July. The eggs hatched until late October. The EPR was significantly correlated with the average monthly temperature. Additional investigation of the egg distributions in the nests showed that most eggs were kept around the royal cell, which contained the reproductives. The largest colony had 109 supplemental queens and 94,023 eggs, suggesting that each queen produced an average of 24.7 eggs per day, based on the known mean hatching period of an inseminated egg of 34.95±0.12 (SE) days.     

Histology of the hormone-producing glands in the damp-wood termite <Emphasis Type="Italic">Hodotermopsis sjostedti</Emphasis> (Isoptera,Termopsidae): A focus on soldier differentiation

Caste differentiation in termites depends on complex hormonal changes during postembryonic development. Juvenile hormone (JH) is a central player in this process. The present study examined histological changes in the main hormone-producing endocrine glands, the corpora allata and molt glands, in the Japanese dampwood termite Hodotermopsis sjostedti. We focused on the soldier caste differentiation pathway, which can be induced artificially using an analogue of JH. The corpora allata exhibited volumetric changes during soldier induction, reflecting variations in the quantity of cytoplasm. Corpora allata from alates and neotenics clearly showed differentiation accompanied by cell proliferation, preparing for the high-level JH production necessary for reproduction. However, the volume increase of corpora allata was not always correlated to high JH titers. In contrast, molt glands degenerated in the reproductive castes. The JH analogue induced hypertrophy of the molt glands, along with the formation of lacunae, possibly related to ecdysteroid production. The JH analogue effect, inducing soldier differentiation, was suggested to require both mimic of high JH titers and stimulation of the molt glands. Received 12 November 2007; revised 2 June 2008; accepted 14 July 2008.     

Bioassay design and length of time in the laboratory affect intercolonial interactions of the Formosan subterranean termite (Isoptera, Rhinotermitidae)

This study examined the effect of diet, experimental design, and length of time in the laboratory on intercolonial agonism among Formosan subterranean termite, Coptotermes formosanus Shiraki, colonies. In pairings of 12 C. formosanus Shiraki colonies collected in an urban forest, there was no significant reduction in survival of termites in 30 out of 59 colony pairs compared to colony controls, but there was <50% survival in 18 colony pairs and <10% survival in six colony pairs. There was no correlation between the level of aggressive behavior and the laboratory diet of the termites. Effect of bioassay design and length of time in the laboratory was evaluated in three colony pairs where tests were first conducted on the day of field collection, then colony pairs were retested every 7 days. Aggressive behavior decreased over time in both bioassays, but it tended to decrease more rapidly in the Petri dish tests. The rapid loss of agonism in groups of termites kept in the laboratory demonstrates that changes in environmental factors affect intercolonial agonism. This article presents the results of research only. Mention of a commercial or proprietary product does not constitute endorsement or recommendation by the USDA.     

Effects of antibiotics on hydrogen production and gut symbionts in the Formosan subterranean termite Coptotermes formosanus (Isoptera: Rhinotermitidae)

Abstract Symbiotic microorganisms that inhabit the gut of Coptotermes formosanus enable this termite to degrade lignocelluloses and further produce hydrogen as an important intermediate to be recycled in its hindgut or as a byproduct to be emitted to the atmosphere. Both symbiotic protists and prokaryotes in the guts of termites demonstrated some different roles with respect to hydrogen production. In this study, the effects of two antibiotics, ampicillin and tetracycline, on hydrogen emission and the gut symbionts of C. formosanus were investigated. Hydrogen emission from termite guts was significantly enhanced when termites fed on wood diets treated with either ampicillin or tetracycline. The greatest H₂ emission rates, 2 519 ± 74 and 2 080 ± 377 nmol/h/g body weight, were recorded with the treatments of ampicillin and tetracycline, respectively, which showed 6–7 times more H₂ production than that of controls. Antibiotic‐treated diets negatively affected the prokaryotic communities and reduced their abundances, particularly on those ectosymbionts inhabiting the gut walls or in the gut fluid of C. formosanus, such as spirochetes. However, no significant reductions in the counts of gut cellulolytic protists, Pseudotrichonympha grassii and Holomastigotoids hartmanni, were recorded; and with a further observation by confocal laser scanning microscopy, the endosymbionts inhabiting P. grassii generally survived the antibiotic treatments. These results suggest that some prokaryotes may serve as the main hydrogen consumers, while P. grassii, together with its endosymbionts, may function as the main contributors for hydrogen production in the hindgut of C. formosanus.     

Comparative studies on alate wing formation in two related species of rotten-wood termites: <Emphasis Type="Italic">Hodotermopsis sjostedti</Emphasis> and <Emphasis Type="Italic">Zootermopsis nevadensis</Emphasis> (Isoptera,Termopsidae)

Summary Termite colonies are comprised of several types of castes that differentiate throughout postembryonic development. In termopsid termites (family Termopsidae), alates are normally differentiated from apterous instars by two nymphal instar stages and three moulting events. Here, we report that of the rotten-wood termite Hodotermopsis sjostedti. There is only a single nymphal instar between the pseudergate and alate stages. During the annual alate production season in June/July, we observed some nymphs with small wing buds which were dorsally swollen. Those nymphal individuals subsequently moulted into alates through only a single moult. We examined their histology and internal morphology and observed that the folding pattern of the newly formed wings was very different from that seen in second stage nymphs of the closely related species Zootermopsis nevadensis. The newly formed wings of H. sjostedti are formed inside the relatively smaller wing buds and therefore must be folded in a complicated manner. Our observations revealed that the tips of the folded wings were elongated and bent, such that they overlapped in the median plane. We suggest that heterochronic evolutionary change accounts for the compression of nymphal development into a single instar. We also suggest that this probably occurred at either the individual or colony level in this species.Received 18 August 2003; revised 11 December 2003; accepted 8 January 2004.     

Changes in endogenous cellulase gene expression levels and reproductive characteristics of primary and secondary reproductives with colony development of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae)

The unique feature of eusociality is reproductive division of labor. At the termite colony initiation stage, there are only reproductives plus larvae and eggs that need to be cared for. As workers increase in number with colony development, reproductives are thought to be relieved of the cost of brood care and able to resume reproduction. This transition of responsibility for the care of offspring from parents to their offspring has been considered as a crucial step in the evolution of termite eusociality (trophic shift model). Here, we studied the endogenous cellulase gene expression levels and reproductive characteristics of alates and primary reproductives at 30, 50, 100, and 400 days after colony foundation in the termite Reticulitermes speratus. As a result, when the numbers of workers reached about 100 (400 days), wood digestion abilities of alates and primary reproductives decreased significantly while ovaries and testis were well developed. Moreover, wood digestion abilities of female secondary reproductives with well-developed ovaries, collected in the field colony, were lower than those of any stages of primary queens. These results were consistent with the trophic shift model, and suggested the importance of switch from parental care to alloparental care for reproductive division of labor and evolution of termite eusociality.     

Taxonomy and distribution of termite fauna (Isoptera) in Riyadh Province,the Kingdom of Saudi Arabia,with an updated list of termite species on the Arabian Peninsula

The present study shows an updated synoptic list of the 30 known Isoptera of the Arabian Peninsula which are classified under four families and nine genera. Twenty-seven species are hitherto known from the Kingdom of Saudi Arabia (KSA). The present inventory of the termites of Riyadh Province (KSA) indicated three species, Anacanthotermes ochraceous (Burmeister 1839), Psammotermes hypostoma Desneux, 1902 and a rare species, Coptotermes heimi (Wasmann 1902). We present an illustrated key to species based on the soldier caste. Anacanthotermes ochraceous, and P. hypostoma are widely distributed Palearctic species whereas C. heimi seems rare and is a new record for KSA. Distribution maps for the three species are provided based on recently collected material and literature records and remarks on species habitat preference are given.     

Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera,Rhinotermitidae)

Summary. Facultative parthenogenesis has great adaptive significance, especially with regard to low pairing efficiency. In the termite Reticulitermes speratus, females that fail to mate with males reproduce parthenogenetically and found colonies cooperatively with partner females or even alone. Comparison of colony foundation success at 400 days between colonies founded by single females (F), female-female pairs (FF), and male-female pairs (FM) showed that female-female cooperation promoted colony survivorship over monogamous foundation. We report here for the first time the mode of parthenogenesis in Isoptera. Combining chromosome observations and genetic analysis using microsatellites, we show that the mode of parthenogenesis is diploid thelytoky and that the restoration of ploidy is most likely accomplished by terminal fusion. Parthenogens show a higher mortality and a longer egg-development time than sexually produced offspring, probably due to reduced heterozygosity. In addition Wolbachia bacteria were detected in R. speratus. However, since Wolbachia was also detected in non-parthenogenetic R. flavipes, it is unlikely that Wolbachia is the cause of parthenogenesis in R. speratus.Received 30 October 2003; revised 4 March 2004; accepted 17 March 2004.     

Modifications in the oviducts of workers and queens of <Emphasis Type="Italic">Melipona quadrifasciata anthidioides</Emphasis> (Hymenoptera: Apidae) with different ages

The study of morphological features of highly eusocial bees has helped to answer a series of questions concerning their biology. The labor division places the females into two castes, queen with reproductive function and worker with a wide variety of tasks. However, in different species and under different conditions, workers can develop ovaries and lay trophic eggs that are eaten by the queen or used to originate males. In this work, the development of the oviducts was monitored in workers and virgin queens of Melipona quadrifasciata anthidioides specimens of different ages to verify whether there is permanent sterility of these queens and workers due to aging. Lateral and common oviducts of virgin queens aged <7, 10, 15, 20, and 25 days old, physogastric queens, nurse, and forager workers were analyzed for histology and ultrastructure. Although the structural organization of the lateral and common oviducts were very similar, differences in width of the cuticle and the degree of chromatin condensation were observed, indicating differences in the development of this organ of the reproductive system between the castes. It was also demonstrated that electron-lucent vesicles appear to be related to the formation of the cuticle that lines the oviducts. Because no cellular death characteristics were found, it can be inferred that the absence of mating of the queens as old as of 25 days of age does not cause permanent sterility.