Asexual queen succession in the subterranean termite Reticulitermes virginicus

Termite colonies are founded by a pair of primary reproductives. In many species, including subterranean termites (family Rhinotermitidae), the primary king and queen can be succeeded by neotenic reproductives that are produced from workers or nymphs within the colony. It is generally believed that these neotenics inbreed within the colony, sometimes for many generations. Here, we show that primary queens of the North American subterranean termite, Reticulitermes virginicus, are replaced by numerous parthenogenetically produced female neotenics. We collected functional female neotenics from five colonies of R. virginicus in North Carolina and Texas, USA. Genetic analysis at eight microsatellite loci showed that 91-100% of the neotenics present within a colony were homozygous at all loci, indicating that they were produced through automictic parthenogenesis with terminal fusion. In contrast, workers, soldiers and alates were almost exclusively sexually produced by mating between the female neotenics and a single king. This is the second termite species shown to undergo asexual queen succession, a system first described in the Japanese species, Reticulitermes speratus. Thus, the conditional use of sexual and asexual reproduction to produce members of different castes may be widespread within Reticulitermes and possibly other subterranean termites.     

The challenge of biomimetic design for carbon-neutral buildings using termite engineering

Abstract The main aim of this paper is to present humanity and termites as design partners in the creation of a new dimension of ecosystem understanding. The paper by Turner and Soar, “Beyond biomimicry: What termites can tell us about realizing the living building” (2008) opens up a new era in how we think of human habitations, not only on earth, but perhaps on other planets, and using the termite model as the corner stone of innovative engineering. We know that termites are masters of constructing ‘buildings’ that meet all nutrition, energy, waste disposal needs, shelter, and food sources for many other animals and insects. We need to emulate the symbiotic abilities of termites to survive over time, for we all live on this symbiotic planet, and symbiosis is natural and common.     

Queen pheromone regulates egg production in a termite

In social insects, resource allocation is a key factor that influences colony survival and growth. Optimal allocation to queens and brood is essential for maximum colony productivity, requiring colony members to have information on the total reproductive power in colonies. However, the mechanisms regulating egg production relative to the current labour force for brood care remain poorly known. Recently, a volatile chemical was identified as a termite queen pheromone that inhibits the differentiation of new neotenic reproductives (secondary reproductives developed from nymphs or workers) in Reticulitermes speratus. The same volatile chemical is also emitted by eggs. This queen pheromone would therefore be expected to act as an honest message of the reproductive power about queens. In this study, we examined how the queen pheromone influences the reproductive rate of queens in R. speratus. We compared the number of eggs produced by each queen between groups with and without exposure to artificial queen pheromone. Exposure to the pheromone resulted in a significant decrease in egg production in both single-queen and multiple-queen groups. This is the first report supporting the role of queen pheromones as a signal regulating colony-level egg production, using synthetically derived compounds in a termite.     

Farmers’ perception of termites in agriculture production and their indigenous utilization in Northwest Benin

Background

Although termites are considered as agricultural pests, they play an important role in maintaining the ecosystem. Therefore, it matters to investigate the farmers’ perception of the impacts of the termites on the agriculture and their indigenous utilization.

Methods

A semi-structured questionnaire was used to interview 94 farmers through 10 villages of Atacora department, in the northwestern region of Benin, to obtain information for the development of successful strategies of termite management and conservation. Their perceptions on the importance and management of termites along with the indigenous nomenclature and utilization of termite mounds were assessed. Termite species identified by farmers were collected and preserved in 80% alcohol for identification.

Results

Eight crops were identified by farmers as susceptible to termites with maize, sorghum, and yam as being the most susceptible. According to farmers, the susceptibility to termites of these crops is due to their high-water content and sweet taste. A total of 27 vernacular names of termites were recorded corresponding to 10 species, Amitermes evuncifer, Macrotermes subhyalinus, and Trinervitermes oeconomus being the most damaging termite species. All the names given to termite species had a meaning. The drought was identified by farmers as the main factor favouring termite attacks. Demolition of termite mounds in the fields was the most commonly reported control method. Salt and other pesticides were commonly used by farmers to protect stored farm products. The lack of effective control methods is the main constraint for termite management. In northwestern Benin, farmers reported different purpose utilizations of termite mounds and termites.

Conclusions

The study has shown that farmers perceived termites as pests of several agricultural crops and apply various indigenous control practices whose efficiency need to be verified. Utilization of termites and termite mound soil as food and medicinal resources underlines the need for a more focused approach to termite control for the conservation of non-pest termite species. The sensitization of farmers on the importance of termites as well as the development of an integrated control method to combat termite pests proved necessary.

     

Infestation of African savanna ecosystems by subterranean termites

This review is an analysis of the dimensions of termite infestation in African savannas. The aim of this work is to draw the attention of ecologists, conservationists, policy makers and farmers to the current and future threats of subterranean termites to the functioning and sustainability of such ecosystem habitats. This study analyzes and describes termite problem (questionable changes in density and assemblage structure) in selected African savannah ecosystems, synthesizes information on the effects of various human induced habitat disturbance regimes on termites’ assemblage structure, predators, nests and feed resources to generate hypotheses relating termite infestation with anthropogenic activities; it describes and critiques existing termite management practices. The review is suggestive that the infestation and resultant undesirable effects of subterranean termites in African savannahs are largely a consequence of the inappropriate savannah management practices (overgrazing, indiscriminate tree cutting and overhunting) undertaken by humans in pursuit of various livelihood options. Based on the evidence presented herein, we hypothesized that (1) human induced habitat disturbance in savanna ecosystems alters the feeding group composition of termites’ assemblages, favoring grass harvesters and polyphagus termite feeders that forage on more abundant food items, paying little attention to rarer food items and (2) habitat disturbance through activities like heavy grazing and overhunting results in decline in the populations of both macro and microscopic termite predators, which eventually enhances the proliferation of termite populations, escalates the density of termite nests particularly epigeal mounds and intensifies consumption of herbaceous savannah vegetation. The review calls for dedicated efforts to develop ecological thresholds of savannah biotic and abiotic ecosystem components in which human induced disturbance regimes trigger the destructive behavior of termites. This would provide information that will act as a precautionary savannah habitat monitoring and decision support tool to prevent future infestation of savannah habitats with termites. Also, the review shows that majority of the termite control practices are ineffective, ecologically unsustainable and above all, do not address the root cause of termite infestation and thus merely provide temporary relief to the problem. As such, termite control methods that attempt to enhance proliferation of termite predators need to be studied, developed and emphasized. This review reveals that human induced habitat disturbance depletes termites’ predator populations, leading to proliferation of termite populations particularly grass harvesters that intensify their consumption on grass biomass and eventually contribute to denudation of herbaceous vegetation cover in savannah ecosystems.     

白蚁诱食信息素研究进展

白蚁为社会性昆虫,其组织结构和联系方式主要由白蚁外分泌腺产生的起诱导和调节白蚁行为反应作用的信息素来获得。由白蚁下唇腺产生的诱食信息素,能够在白蚁巢体的群体性食物采集中诱使取食白蚁形成聚集,并且取食食物的相同位置,从而提高白蚁巢体采集食物的效率。目前,已确定对苯二酚为白蚁诱食信息素,且认为整个等翅目昆虫都产生和使用对苯二酚作为诱食信息素,与分类地位和生物学特性无关。该文概述了白蚁诱食信息素的分泌器官、种特异性、生物学意义、生物合成途径及其在白蚁防治中的应用等方面的研究进展。     

Termite-egg mimicry by a sclerotium-forming fungus

Mimicry has evolved in a wide range of organisms and encompasses diverse tactics for defence, foraging, pollination and social parasitism. Here, I report an extraordinary case of egg mimicry by a fungus, whereby the fungus gains competitor-free habitat in termite nests. Brown fungal balls, called 'termite balls', are frequently found in egg piles of Reticulitermes termites. Phylogenetic analysis illustrated that termite-ball fungi isolated from different hosts (Reticulitermes speratus, Reticulitermes flavipes and Reticulitermes virginicus) were all very similar, with no significant molecular differences among host species or geographical locations. I found no significant effect of termite balls on egg survivorship. The termite-ball fungus rarely kills termite eggs in natural colonies. Even a termite species (Reticulitermes okinawanus) with no natural association with the fungus tended termite balls along with its eggs when it was experimentally provided with termite balls. Dummy-egg bioassays using glass beads showed that both morphological and chemical camouflage were necessary to induce tending by termites. Termites almost exclusively tended termite balls with diameters that exactly matched their egg size. Moreover, scanning electron microscopic observations revealed sophisticated mimicry of the smooth surface texture of eggs. These results provide clear evidence that this interaction is beneficial only for the fungus, i.e. termite balls parasitically mimic termite eggs.     

Sampling subterranean termite species diversity and activity in tropical savannas: an assessment of different bait choices

Abstract.  1. Cellulose baits are commonly used for semi-quantitative sampling of subterranean wood-feeding termites, with a single food choice sampling programme implemented most often. In most situations, however, the composition and feeding preferences of the subterranean termite assemblage remain unknown.
2. The diversity, frequency, foraging activity, and intensity of attack of termites were assessed regularly at 144 baits representing 12 different bait choices over 8.5 months, in two northern Australian tropical savanna sites that differed in vegetation structure (closed vs open). Baits differed in type (paper rolls, cardboard, wooden stakes), position (surface, buried), and moisture status at installation (wet, dry).
3. Sixteen species were recorded, including 11 wood-feeders. Average species diversity, foraging activity, and bait consumption were greater at buried baits than at surface baits. Wooden baits were most attractive early in the experiment, and paper baits more attractive later. Mean species diversity was greatest at wooden stakes in the closed site. Species frequency of occurrence varied across bait choices.
4. A composite bait sampling protocol of stakes and paper rolls installed above and below ground gave an accurate assessment of the activity, diversity, and structure of the termite guild sampled across all baits over 8.5 months.
5. The choice of bait, its presentation, and time of examination are critical to the success of a termite baiting programme. If the aim is to characterise the structure and foraging activity of the subterranean termite assemblages that are attracted to baits, composite baiting protocols should be implemented.     

Detection of Mitochondrial COII DNA Sequences in Ant Guts as a Method for Assessing Termite Predation by Ants

Termites and ants contribute more to animal biomass in tropical rain forests than any other single group and perform vital ecosystem functions. Although ants prey on termites, at the community level the linkage between these groups is poorly understood. Thus, assessing the distribution and specificity of ant termitophagy is of considerable interest. We describe an approach for quantifying ant-termite food webs by sequencing termite DNA (cytochrome c oxidase subunit II, COII) from ant guts and apply this to a soil-dwelling ant community from tropical rain forest in Gabon. We extracted DNA from 215 ants from 15 species. Of these, 17.2 % of individuals had termite DNA in their guts, with BLAST analysis confirming the identity of 34.1 % of these termites to family level or better. Although ant species varied in detection of termite DNA, ranging from 63 % (5/7; Camponotus sp. 1) to 0 % (0/7; Ponera sp. 1), there was no evidence (with small sample sizes) for heterogeneity in termite consumption across ant taxa, and no evidence for species-specific ant-termite predation. In all three ant species with identifiable termite DNA in multiple individuals, multiple termite species were represented. Furthermore, the two termite species that were detected on multiple occasions in ant guts were in both cases found in multiple ant species, suggesting that ant-termite food webs are not strongly compartmentalised. However, two ant species were found to consume only Anoplotermes-group termites, indicating possible predatory specialisation at a higher taxonomic level. Using a laboratory feeding test, we were able to detect termite COII sequences in ant guts up to 2 h after feeding, indicating that our method only detects recent feeding events. Our data provide tentative support for the hypothesis that unspecialised termite predation by ants is widespread and highlight the use of molecular approaches for future studies of ant-termite food webs.     

Evidence for genetically influenced caste determination in phylogenetically diverse species of the termite genus Reticulitermes

A number of social insect species have recently been shown to have genetically influenced caste determination (GCD), challenging the conventional view that caste determination should be strictly environmental. To date, GCD has been found in phylogenetically isolated species; examples of GCD being present in multiple species of a genus are lacking. Through crossing experiments of neotenic (juvenile) reproductives, we have recently provided the first evidence for a royal versus worker GCD in the termite Reticulitermes speratus. To elucidate whether this system is more widespread, we performed crossing experiments using three additional Reticulitermes species. Offspring caste and sex ratios were found to be highly similar to those found previously in R. speratus, raising the possibility that GCD was present in an ancestral lineage of Reticulitermes, and subsequently maintained throughout several episodes of speciation.     

Termite Feeding by <Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis> at Bai Hokou,Central African Republic

Though insectivory by large-bodied gorillas may be unexpected, researchers have reported it in all populations of gorillas studied to date. Our study of 2 well monitored groups of western gorillas (Gorilla gorilla gorilla) at Bai Hokou in Dzanga-Ndoki National Park, Central African Republic provides information on frequency and variability of termite consumption (the most commonly eaten insect) as well as some of the first direct observations of the behavior. Pooled data from both groups indicate termite feeding on 34% and 83% of days, through fecal analysis and feeding trails, respectively. Direct observations revealed that termite feeding occurred on 91% of the days for 1 group, in which the silverback fed on termites during 13% of all feeding scans, making termites the most commonly observed food item. The group that had a higher density of termite mounds in its home range consumed termites more frequently than the other group did. A higher proportion of fecal samples from the silverbacks contained termite remains than the ones from adult females and juveniles. Termite consumption was lower during the dry season, but it does not correlate with rainfall, measures of fruit availability, or fruit consumption. Displacements at termite mounds occurred more than expected, indicating that they are a patchy, sought-after food resource. Gorillas did not use tools to extract termites, but they used 2 different techniques to remove them from the cells. Though culture or social traditions may cause the variation in termite consumption across sites, further investigation of termite availability and consumption is necessary to rule out ecological and methodological explanations for observed variations.     

Methods to mark termites with protein for mark–release–recapture and mark–capture type studies

Studies were conducted to investigate the feasibility of marking the southwestern desert subterranean termite, Heterotermes aureus (Snyder), with rabbit immunoglobulin G (IgG) protein for mark–release–recapture (MRR) and mark–capture type studies. Qualitative laboratory studies were conducted to determine how long reagent-grade rabbit IgG is retained on or in H. aureus that were marked either externally with a topical spray, internally by feeding them a rabbit IgG-marked food source, or both internally and externally (double marked). Marked termites were detected by an anti-rabbit IgG enzyme-linked immunosorbent assay. Data indicated that the termites retained the mark for at least 35 days, regardless of the marking procedure. A second series of laboratory studies were conducted to determine how fast H. aureus acquire the mark after feeding on cardboard bait that was either sprayed or soaked in different formulations of rabbit IgG. The IgGs tested were a highly purified and costly reagent grade IgG at 5.0 mg/ml and a less pure and less costly technical grade rabbit IgG at 1.0 mg/ml. The results showed that termites acquired both marks equally well after exposure to the soaked cardboard treatment. The advantages and limitations of protein marking termites with rabbit IgG for MRR or mark–capture termite studies are discussed.     

Asexual queen succession in the higher termite Embiratermes neotenicus

Asexual queen succession (AQS), in which workers, soldiers and dispersing reproductives are produced sexually while numerous non-dispersing queens arise through thelytokous parthenogenesis, has recently been described in three species of lower termites of the genus Reticulitermes. Here, we show that AQS is not an oddity restricted to a single genus of lower termites, but a more widespread strategy occurring also in the most advanced termite group, the higher termites (Termitidae). We analysed the genetic structure in 10 colonies of the Neotropical higher termite Embiratermes neotenicus (Syntermitinae) using five newly developed polymorphic microsatellite loci. The colonies contained one primary king accompanied either by a single primary queen or by up to almost 200 neotenic queens. While the workers, the soldiers and most future dispersing reproductives were produced sexually, the non-dispersing neotenic queens originated through thelytokous parthenogenesis of the founding primary queen. Surprisingly, the mode of thelytoky observed in E. neotenicus is most probably automixis with central fusion, contrasting with the automixis with terminal fusion documented in Reticulitermes. The occurrence of AQS based on different mechanisms of ploidy restoration raises the hypothesis of an independent evolutionary origin of this unique reproductive strategy in individual lineages of lower and higher termites.     

Insect antifeedants, pterocarpans and pterocarpol, in heartwood of Pterocarpus macrocarpus Kruz

The insect antifeedant activities of pterocarpans and a sesquiterpene alcohol from the dichloromethane extract of Pterocarpus macrocarpus Kruz. (Leguminosae) were evaluated against the common cutworm, Spodoptera litura F. (Noctuidae), and the subterranean termite, Reticulitermes speratus (Kolbe)(Rhinotermitidae). Three pterocarpans, (-)-homopterocarpin (1), (-)-pterocarpin (2), and (-)-hydroxyhomopterocarpin (3) and the sesquiterpene alcohol, (+)-pterocarpol (5), were isolated from the dichloromethane extract of the heartwood of P. macrocarpus under guidance by a biological assay. Among these natural products, the most active insect antifeedant against both S. litura and R. speratus was 1. On the other hand, sesquiterpene alcohol 5 showed less insect antifeedant activity than the other pterocarpans against both insect species. While its methylated derivative, (-)-methoxyhomopterocarpin (4), showed high biological activity, 3 showed less insect antifeedant activity in this study. Interestingly, racemic 1 did not show insect antifeedant activity against S. litura. However, all of the test pterocarpans and isoflavones showed antifeedant activity against the test termites. Additionally, since these compounds were major constituents of P. macrocarpus, these antifeedant phenolics may act as chemical defense factors in this tree. In Thailand, lumber made from this tree is used to make furniture and in building construction due to its resistance to termite attack.     

Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites

The molecular phylogeny of methanogenic archaea associated with the flagellated protist species Dinenympha and Microjoenia in the gut of termites, Reticulitermes speratus and Hodotermopsis sjoestedti, and those attached to the gut epithelium was examined based on PCR-amplified small-subunit ribosomal RNA genes. The sequences identified were classified into six groups within the genus Methanobrevibacter, including groups of yet uncharacterized novel species. Closely related methanogens were shared between Microjoenia and some Dinenympha cells in each termite. The methanogens harbored by the flagellates were phylogenetically different from the methanogens associated with the gut epithelium, suggesting that distinct methanogen species showed distinct spatial distributions in the termite gut.     

Termiticidal activity of diterpenes from the roots of Euphorbia kansui

Five ingenane compounds, 1-5, kansuinins A and B, isolated from Euphorbia kansui, and their derivatives 7 and 9 were tested for termiticidal activity against the Japanese termite, Reticulitermes speratus. At 72 hours after treatment, the ingenane compounds 1 to 5 caused 100% mortality in R. speratus at 50, 25 and 12.5 microg/disk, respectively, except for compound 1, which gave a mortality rate of (93.06 +/- 5.56)% at 12.5 microg/disk. At 36, 48 and 60 hours after treatment, compounds 1 to 5 showed more termiticidal activity than kansuinins A and B and their derivatives. The kansuinins showed no or only slight activity against termites in the filter paper bioassay under the conditions tested compared with a solvent control.     

Identification of two subterranean termite species (Isoptera: Rhinotermitidae) using cellulase genes

To identify subterranean termite species, we designed a pair of common primers that amplified 381-bp fragments from cDNAs encoding the endo-beta-1,4-glucanases (EGases) of Coptotermes formosanus Shiraki and Reticulitermes speratus (Kolbe). cDNAs from C. formosanus and R. speratus, and genomic DNA from R. speratus, were amplified by polymerase chain reaction (PCR) by using this primer pair and then cloned and sequenced. Sequences amplified from C.formosanus cDNA displayed 97-99% identity to cDNA encoding the EGase of C. formosanus (CfEG), and 92-94% identity to cDNA encoding the EGase of R. speratus (RsEG). By contrast, cDNA from R. speratus displayed 99-100% identity to RsEG cDNA and 93-94% identity to CfEG cDNA. CfEG and RsEG cDNAs can therefore be used as markers for the identification of these termite species. This is the first report of the successful identification of termite species by using cDNA and genomic DNA sequences of termite origin.     

Interactions between wood-inhabiting fungi and termites: a meta-analytical review

The foraging behavior and survivorship of termites are modified by the presence of wood-inhabiting fungi. Nonetheless, it is not clear if these interactions are beneficial, negative, or neutral for termites. We conducted a meta-analytical review to determine if the presence of wood-inhabiting fungi affects the foraging behavior and survivorship of termites. Overall, the presence of wood-inhabiting fungi in a resource used by termites was positive, increasing resource consumption by 120%, and aggregation behavior by 81%. The presence of fungi also increased termite trail-following by approximately 200% and increased survival by 136%. The results varied, however, according to the type of fungi evaluated. Decay fungi and sap-stain fungi elicited positive responses in termites, whereas molds did not affect the consumption of cellulose by termites. Amongst the decay fungi group, white-rot fungi caused the strongest and most positive response in all termite behaviors evaluated, although brown-rot fungi is known to be preferred by termites. The results of our study, therefore, suggest that wood-inhabiting fungi are potential facilitators of the foraging behavior and survivorship of termites. These results have great implications for termite biocontrol, as well as for knowledge of the ecological aspects of termite–fungi interactions.     

Repellent and toxic effects of plant extracts on subterranean termites (Isoptera: Rhinotermitidae).

The effects of four plant extract formulations on the orientation and survival of subterranean termites were tested. In choice experiments, extract-treated filter paper had a significantly repellent effect on groups of Reticulitermes santonensis De Feytaud, R. virginicus (Banks), Coptotermes formosanus Shiraki, and Schedorhinotermes intermedius Breinli. There was no species-specific difference in avoidance behavior toward the tested concentrations. No-choice experiments revealed toxic properties of all investigated extracts by contact or airborne compounds against R. santonensis. However, high termite mortality was only achieved by forced direct or forced indirect exposure to the plant material, Feeding deterrence or digestive toxicity could not be judged in these experiments. One of the extracts was efficiently used for soil treatments to protect a food substrate against R. santonenis infestation. Extract-treated barriers in the experiments did not affect mortality compared with control trials but prevented termites from penetrating treated soil.