Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles

In this study, we examine gene diversity for formyl-tetrahydrofolate synthetase (FTHFS), a key enzyme in homoacetogenesis, recovered from the gut microbiota of six species of higher termites. The "higher" termites (family Termitidae), which represent the majority of extant termite species and genera, engage in a broader diversity of feeding and nesting styles than the "lower" termites. Previous studies of termite gut homoacetogenesis have focused on wood-feeding lower termites, from which the preponderance of FTHFS sequences recovered were related to those from acetogenic treponemes. While sequences belonging to this group were present in the guts of all six higher termites examined, treponeme-like FTHFS sequences represented the majority of recovered sequences in only two species (a wood-feeding Nasutitermes sp. and a palm-feeding Microcerotermes sp.). The remaining four termite species analyzed (a Gnathamitermes sp. and two Amitermes spp. that were recovered from subterranean nests with indeterminate feeding strategies and a litter-feeding Rhynchotermes sp.) yielded novel FTHFS clades not observed in lower termites. These termites yielded two distinct clusters of probable purinolytic Firmicutes and a large group of potential homoacetogens related to sequences previously recovered from the guts of omnivorous cockroaches. These findings suggest that the gut environments of different higher termite species may select for different groups of homoacetogens, with some species hosting treponeme-dominated homoacetogen populations similar to those of wood-feeding, lower termites while others host Firmicutes-dominated communities more similar to those of omnivorous cockroaches.     

Identifying the core microbial community in the gut of fungus‐growing termites

Gut microbes play a crucial role in decomposing lignocellulose to fuel termite societies, with protists in the lower termites and prokaryotes in the higher termites providing these services. However, a single basal subfamily of the higher termites, the Macrotermitinae, also domesticated a plant biomass‐degrading fungus (Termitomyces), and how this symbiont acquisition has affected the fungus‐growing termite gut microbiota has remained unclear. The objective of our study was to compare the intestinal bacterial communities of five genera (nine species) of fungus‐growing termites to establish whether or not an ancestral core microbiota has been maintained and characterizes extant lineages. Using 454‐pyrosequencing of the 16S rRNA gene, we show that gut communities have representatives of 26 bacterial phyla and are dominated by Firmicutes, Bacteroidetes, Spirochaetes, Proteobacteria and Synergistetes. A set of 42 genus‐level taxa was present in all termite species and accounted for 56–68% of the species‐specific reads. Gut communities of termites from the same genus were more similar than distantly related species, suggesting that phylogenetic ancestry matters, possibly in connection with specific termite genus‐level ecological niches. Finally, we show that gut communities of fungus‐growing termites are similar to cockroaches, both at the bacterial phylum level and in a comparison of the core Macrotermitinae taxa abundances with representative cockroach, lower termite and higher nonfungus‐growing termites. These results suggest that the obligate association with Termitomyces has forced the bacterial gut communities of the fungus‐growing termites towards a relatively uniform composition with higher similarity to their omnivorous relatives than to more closely related termites.     

Identification of multi‐component trail pheromones in the most evolutionarily derived termites,the Nasutitermitinae (Termitidae)

In the present study, trail pheromone blends are identified for the first time in termites. In the phylogenetically complex Nasutitermitinae, trail‐following pheromones are composed of dodecatrienol and neocembrene, the proportions of which vary according to species, although neocembrene is always more abundant than dodecatrienol (by 25–250‐fold). Depending on species, termites were more sensitive to dodecatrienol or to neocembrene but the association of both components always elicited significantly higher trail following, with a clear synergistic effect in most of the studied species. A third component, trinervitatriene, was identified in the sternal gland secretion of several species, but its function remains unknown. The secretion of trail pheromone blends appears to be an important step in the evolution of chemical communication in termites. The pheromone optimizes foraging, and promotes their ecological success. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 20–27.     

Morphological phylogenetics of termites (Isoptera)

Isoptera (termites) are an ecologically important order, with both a high abundance and biomass in tropical ecosystems. However, there have been few phylogenetic hypotheses for termites, and we present here the first comprehensive cladistic analysis for the group. We analysed relationships between all seven termite families, including representatives of all known feeding group, plus a number of systematically critical taxa. Termite species richness is biased towards the higher termites (Termitidae), and our taxon sampling reflects this. Our analysis was based essentially on morphological characters (96 workers, 93 soldiers) plus seven biological characters. The cladistic analysis gave four equally parsimonious trees, representing two islands of topologies. The strict consensus tree is fully resolved for the higher termites, but less so for the lower termites. Overall there is low statistical support for the suggested topology, and this can be explained by the high incongruence between the data sets (worker, soldier and biological). This study highlights the particular problems of coding morphological characters in social insects with multiple castes. Without the input of additional data sets, e.g. alates, biological, behavioural and molecular, it will not be possible to obtain a well-supported termite phylogeny.     

Influence of termites on the soil seed bank in an African savannah

In savannah ecosystems, termites drive key ecosystem processes, such as primary production through creation of patchiness in soil nutrients availability around their nests. In this study, we evaluated the role of termites in altering the soil seed bank size, an important ecosystem component that has often been overlooked in previous work. Data on above ground vegetation and soil seed bank samples were collected from four microhabitats, that is, the wooded mound, unwooded mound, tree sub‐canopy and the open grassland matrix in a protected game reserve in south‐central Zimbabwe. The seedling emergence method was then used to identify species present in the soil samples. One‐way analysis of variance followed by Tukey's multiple comparison tests was executed to test for significant differences in plant species richness among the four microhabitats. The results indicate that plant species richness was high on wooded termite mound but did not differ between the unwooded and the sub‐canopy microhabitats. The open grassland microhabitat had the lowest plant species richness. The influence of termites on the soil seed bank composition was also life form specific. The herb and woody life forms had significantly (α = 0.05) higher species richness in the soil seed bank at wooded and unwooded termite mounds when compared to the other two microhabitats. Overall, these results imply that termites alter the soil seed bank and the findings enhance our understanding of the significant role termites play in regulating processes in savannah ecosystem.     

Hidden cellulases in termites: revision of an old hypothesis

The intestinal flagellates of termites produce cellulases that contribute to cellulose digestion of their host termites. However, 75% of all termite species do not harbour the cellulolytic flagellates; the endogenous cellulase secreted from the midgut tissue has been considered a sole source of cellulases in these termites. Using the xylophagous flagellate-free termites Nasutitermes takasagoensis and Nasutitermes walkeri, we successfully solubilized cellulases present in the hindgut pellets. Zymograms showed that the hindguts of these termites possessed several cellulases and contained up to 59% cellulase activity against crystalline cellulose when compared with the midgut. Antibiotic treatment administered to N. takasagoensis significantly reduced cellulase activity in the hindgut, suggesting that these cellulases were produced by symbiotic bacteria.     

Captive breeding of pangolins: current status,problems and future prospects

Pangolins are unique placental mammals with eight species existing in the world, which have adapted to a highly specialized diet of ants and termites, and are of significance in the control of forest termite disaster. Besides their ecological value, pangolins are extremely important economic animals with the value as medicine and food. At present, illegal hunting and habitat destruction have drastically decreased the wild population of pangolins, pushing them to the edge of extinction. Captive breeding is an important way to protect these species, but because of pangolin’s specialized behaviors and high dependence on natural ecosystem, there still exist many technical barriers to successful captive breeding programs. In this paper, based on the literatures and our practical experience, we reviewed the status and existing problems in captive breeding of pangolins, including four aspects, the naturalistic habitat, dietary husbandry, reproduction and disease control. Some recommendations are presented for effective captive breeding and protection of pangolins.     

Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites?

The mutualism between fungus-growing termites (Macrotermitinae) and their mutualistic fungi (Termitomyces) began in Africa. The fungus-growing termites have secondarily colonized Madagascar and only a subset of the genera found in Africa is found on this isolated island. Successful long-distance colonization may have been severely constrained by the obligate interaction of the termites with fungal symbionts and the need to acquire these symbionts secondarily from the environment for most species (horizontal symbiont transmission). Consistent with this hypothesis, we show that all extant species of fungus-growing termites of Madagascar are the result of a single colonization event of termites belonging to one of the only two groups with vertical symbiont transmission, and we date this event at approximately 13 Mya (Middle/Upper Miocene). Vertical symbiont transmission may therefore have facilitated long-distance dispersal since both partners disperse together. In contrast to their termite hosts, the fungal symbionts have colonized Madagascar multiple times, suggesting that the presence of fungus-growing termites may have facilitated secondary colonizations of the symbiont. Our findings indicate that the absence of the right symbionts in a new environment can prevent long-distance dispersal of symbioses relying on horizontal symbiont acquisition.     

Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.)

Soil-feeding termites play important roles in the dynamics of carbon and nitrogen in tropical soils. Through the mineralization of nitrogenous humus components, their intestinal tracts accumulate enormous amounts of ammonia, and nitrate and nitrite concentrations are several orders of magnitude above those in the ingested soil. Here, we studied the metabolism of nitrate in the different gut compartments of two Cubitermes and one Ophiotermes species using (15)N isotope tracer analysis. Living termites emitted N(2) at rates ranging from 3.8 to 6.8 nmol h(-1) (g fresh wt.)(-1). However, in homogenates of individual gut sections, denitrification was restricted to the posterior hindgut, whereas nitrate ammonification occurred in all gut compartments and was the prevailing process in the anterior gut. Potential rates of nitrate ammonification for the entire intestinal tract were tenfold higher than those of denitrification, implying that ammonification is the major sink for ingested nitrate in the intestinal tract of soil-feeding termites. Because nitrate is efficiently reduced already in the anterior gut, reductive processes in the posterior gut compartments must be fuelled by an endogenous source of oxidized nitrogen species. Quite unexpectedly, we observed an anaerobic oxidation of (15)N-labelled ammonia to nitrite, especially in the P4 section, which is presumably driven by ferric iron; nitrification and anammox activities were not detected. Two of the termite species also emitted substantial amounts of N(2) O, ranging from 0.4 to 3.9 nmol h(-1) (g fresh wt.)(-1), providing direct evidence that soil-feeding termites are a hitherto unrecognized source of this greenhouse gas in tropical soils.     

The fine structural organization of sternal glands of pseudergates and workers in termites (Isoptera): a comparative survey

Thirty-nine species belonging to different families of termites are studied to give a comprehensive view of the evolution of the sternal glands. Several modifications occurring at cuticular and cytological levels are described in neuter castes. The outer epicuticle is always pierced by epicuticular pores. In advanced termites the epicuticular filaments greatly increase in number and length creating a thick layer. The pore canals gradually enlarge while the cuticle changes into a lattice structure lining an extracellular space in which the secretion is stored. Two classes of cells are present in basal termites (Mastotermitidae, Hodotermitidae, Termopsidae and Kalotermitidae) but their glandular structures greatly differ between families. A more complex organization with three classes of cells is found in the Serritermitidae and Rhinotermitidae. A regressive evolution occurs in the Termitidae where only two classes of cells are present. A dual nervous control (campaniform sensilla and neurosecretory fibers) is found in lower termites, except for the Hodotermitidae which have mechanosensory bristles. In the other families, neurosecretory fibers are lacking. A comparison with phylogenetic data is given. A more versatile role of sternal glands in neuter castes is hypothesized.     

白蚁踪迹信息素研究进展

近年来, 固相微萃取技术的使用显著促进了白蚁踪迹信息素研究的开展。目前, 已有77种白蚁的踪迹信息素得到研究, 常见化学成分为十二碳单烯醇、 十二碳二烯醇和十二碳三烯醇, 其次为新松柏烯。已经鉴定的踪迹信息素主要为单组分或双组分系统。白蚁踪迹信息素由腹板腺分泌, 除澳白蚁科的达氏澳白蚁Mastotermes darwiniensis具有3个腹板腺外, 现存的白蚁均具有1个腹板腺, 位于第4或第5腹节。所有腹板腺都具有类型Ⅰ和Ⅱ两类细胞, 原白蚁亚科（Termopsinae）、 齿白蚁科（Serritermitidae）、 鼻白蚁科（Rhinotermitidae）种类的腹板腺还具有类型Ⅲ细胞。踪迹信息素的生物合成还缺乏研究, 推测有甲羟戊酸、 脂肪醇和饱和表皮烃3种途径。白蚁踪迹信息素的简约性十分显著, 不同地理分布、 生物生态习性以及一些系统距离较远的种类具有相同和密切相关的踪迹信息素。对于许多种类, 相同的信息化合物具有踪迹信息素和配对性信息素双重功能。白蚁踪迹信息素种特异性和简约性的适应意义和进化机制需要进一步研究。     

Diversity of fungus‐growing termites (Macrotermes) and their fungal symbionts (Termitomyces) in the semiarid Tsavo Ecosystem,Kenya

Fungus‐growing termites of the subfamily Macrotermitinae together with their highly specialized fungal symbionts (Termitomyces) are primary decomposers of dead plant matter in many African savanna ecosystems. The termites provide crucial ecosystem services also by modifying soil properties, translocating nutrients, and as important drivers of plant succession. Despite their obvious ecological importance, many basic features in the biology of fungus‐growing termites and especially their fungal symbionts remain poorly known, and no studies have so far focused on possible habitat‐level differences in symbiont diversity across heterogeneous landscapes. We studied the species identities of Macrotermes termites and their Termitomyces symbionts by excavating 143 termite mounds at eight study sites in the semiarid Tsavo Ecosystem of southern Kenya. Reference specimens were identified by sequencing the COI region from termites and the ITS region from symbiotic fungi. The results demonstrate that the regional Macrotermes community in Tsavo includes two sympatric species (M. subhyalinus and M. michaelseni) which cultivate and largely share three species of Termitomyces symbionts. A single species of fungus is always found in each termite mound, but even closely adjacent colonies of the same termite species often house evolutionarily divergent fungi. The species identities of both partners vary markedly between sites, suggesting hitherto unknown differences in their ecological requirements. It is apparent that both habitat heterogeneity and disturbance history can influence the regional distribution patterns of both partners in symbiosis.     

Selection on an antimicrobial peptide defensin in ants

Ants live in crowded nests with interacting individuals, which makes them particularly prone to infectious diseases. The question is, how do ants cope with the increased risk of pathogen transmission due to sociality? We have studied the molecular evolution of defensin, a gene encoding an antimicrobial protein, in ants. Defensin sequences from several ant species were analyzed with maximum likelihood models of codon substitution to infer selection. Positive selection was detected in the mature region of defensin, whereas the signal and pro regions seem to be evolving neutrally. We also found a significantly higher rate of nonsynonymous substitutions in some phylogenetic lineages, as well as dN/dS >1, suggesting varying selection pressures in different lineages. Earlier studies on the molecular evolution of insect antimicrobial peptide genes have focused on termites and dipteran species, and detected positive selection only in duplicated termicin genes in termites. These findings, together with our present results, provide an indication that the immune systems of social insects (ants and termites) and dipteran insects may have responded differently to the selection pressure caused by microbial pathogens.     

Male or female soldiers? An evaluation of several factors which may influence soldier sex ratio in lower termites

In termites, the soldiers’ sex ratio is often biased toward one sex. Unlike in the Hymenoptera, this bias cannot easily be explained by relatedness asymmetries because termites are diploid. Matsuura proposed that when large body size is adaptive for colony defence (e.g. in case of phragmotic defence) then the larger sex (given sexual size dimorphism exists) should be more likely to reach a threshold size and develop into soldiers. This would explain biased sex ratios. Matsuura validated his hypothesis for four Reticulitermes species. Here, we tested his hypothesis for two species of Cryptotermes with phragmotic defence. These drywood termites have a life type that is thought to be ancestral in termite’s evolution, thus giving us potential insights into the evolution of the soldier caste. In one of these species, the sex ratio of soldiers was highly female biased, but we could not support Matsuura’s hypothesis. Both species lacked sexual size dimorphism in all castes. Additionally, in both species, the sex ratio of helpers and sexuals did not deviate from a 1:1 ratio, and hence can also not account for the bias observed in soldiers. However, this study showed that there were behavioural differences between the sexes in both species, which could shed some light on biased sex ratio in soldiers. Our findings also indicate that the developmental pathway taken by individuals reflects a ‘decision’ at the colony level. The discovery of behavioural differences between sexes in termites should open the way to similar studies in other taxa with helpers/ workers of both sexes, as it might reveal more task partitioning in colonies than previously thought and it raises questions concerning the selective pressures that acted on caste evolution in termites. Received 30 October 2007; revised 17 January and 27 February; accepted 4 March 2008.     

The structure of termite communities in the Australian tropics

The distributions of 50 species of termites across five habitat types in Kakadu National Park are described. Open forests are richest in species and monsoon forests are species-poor. The greatest diversity of termites is associated with infertile soils and is probably related to the enhanced role of termites in these nutrientimpoverished sites. Only the richness of livewood feeders is associated with disturbance in the form of water buffalo impact. Few relationships with physical characteristics of the soil were apparent. Comparisons between continents suggest that lower termites are richer in Australia than on other continents. There are fewer species of soil-feeding termites, but only two of the four subfamilies of the higher termites (Termitidae) are present in Australia. There appears to be a complementary distribution of areas of high diversity of termites and native herbivorous mammals. This may be due to the ability of termites and other invertebrate groups to exploit low fertility systems and has profound implications for the size structure of the vertebrate community.     

Ant‐termite interactions: an important but under‐explored ecological linkage

Animal interactions play an important role in understanding ecological processes. The nature and intensity of these interactions can shape the impacts of organisms on their environment. Because ants and termites, with their high biomass and range of ecological functions, have considerable effects on their environment, the interaction between them is important for ecosystem processes. Although the manner in which ants and termites interact is becoming increasingly well studied, there has been no synthesis to date of the available literature. Here we review and synthesise all existing literature on ant–termite interactions. We infer that ant predation on termites is the most important, most widespread, and most studied type of interaction. Predatory ant species can regulate termite populations and subsequently slow down the decomposition of wood, litter and soil organic matter. As a consequence they also affect plant growth and distribution, nutrient cycling and nutrient availability. Although some ant species are specialised termite predators, there is probably a high level of opportunistic predation by generalist ant species, and hence their impact on ecosystem processes that termites are known to provide varies at the species level. The most fruitful future research direction will be to evaluate the impact of ant–termite predation on broader ecosystem processes. To do this it will be necessary to quantify the efficacy both of particular ant species and of ant communities as a whole in regulating termite populations in different biomes. We envisage that this work will require a combination of methods, including DNA barcoding of ant gut contents along with field observations and exclusion experiments. Such a combined approach is necessary for assessing how this interaction influences entire ecosystems.     

Odor Aversion and Pathogen-Removal Efficiency in Grooming Behavior of the Termite Coptotermes formosanus

The results of biocontrol with entomopathogens in termites have been discouraging because of the strong social hygiene behavior for removing pathogens from termite colonies. However, the mechanism of pathogen detection is still unclear. For the successful application of biopesticides to termites in nature, it would be beneficial to identify substances that could disrupt the termite’s ability to perceive pathogens. We hypothesized that termites can perceive pathogens and this ability plays an important role in effective hygiene behavior. In this study, pathogen-detection in the subterranean termite Coptotermes formosanus was investigated. We performed quantitative assays on conidia removal by grooming behavior using epifluoresence microscopy and Y-maze tests to examine the perception of fungal odor by termites. Three species each of high- and low-virulence entomopathogenic fungi were used in each test. The results demonstrated that termites removed conidia more effectively from a nestmate’s cuticle if its odor elicited stronger aversion. Highly virulent pathogens showed higher attachment rates to termite surfaces and their odors were more strongly avoided than those of low-virulence isolates in the same species. Moreover, termites appeared to groom each other more persistently when they had more conidia on their bodies. In brief, insect perception of pathogen-related odor seems to play a role in the mechanism of their hygiene behavior.     

Can shifts in metabolic scaling predict coevolution between diet quality and body size?

Larger species tend to feed on abundant resources, which nonetheless have lower quality or degradability, the so‐called Jarman‐Bell principle. The “eat more” hypothesis posits that larger animals compensate for lower quality diets through higher consumption rates. If so, evolutionary shifts in metabolic scaling should affect the scope for this compensation, but whether this has happened is unknown. Here, we investigated this issue using termites, major tropical detritivores that feed along a humification gradient ranging from dead plant tissue to mineral soil. Metabolic scaling is shallower in termites with pounding mandibles adapted to soil‐like substrates than in termites with grinding mandibles adapted to fibrous plant tissue. Accordingly, we predicted that only larger species of the former group should have more humified, lower quality diets, given their higher scope to compensate for such a diet. Using literature data on 65 termite species, we show that diet humification does increase with body size in termites with pounding mandibles, but is weakly related to size in termites with grinding mandibles. Our findings suggest that evolution of metabolic scaling may shape the strength of the Jarman‐Bell principle.     

Termite diversity along a land use intensification gradient in a semi-arid savanna

Disturbance, particularly agricultural expansion is one of the major threats to the biodiversity and ecological functions of tropical and sub-tropical ecosystems. In this regard, we examined changes in the species richness, abundance, and diversity of termites across different disturbance treatments in a sub-tropical semi-arid savanna in south eastern Zimbabwe. Nine transects (100?×?2 m) representing three habitat disturbance treatments (primary woodland; grazing area; agricultural field) were sampled for termites using a rapid biodiversity assessment protocol. Termites were more abundant and species-rich in primary woodland and grazing area than in the agricultural field. Twelve termite species from three sub-families were present, with Microtermes sp. constituting 35% of the identified termite species. Termite feeding group structure differed significantly among land-use types, and of all termites present, wood-feeding termites were the most abundant while soil-feeders were rare in the agricultural field. In conclusion the observed pattern in termite species richness and relative abundance indicates that termites are very resilient to natural disturbance and might actually benefit from some natural disturbances like they did in the grazing area of this study, but they are not resilient to extreme anthropogenic disturbance. Although there was no notable difference in termite species richness and relative abundance between agricultural field and primary woodland, the pattern observed across the three sites may be potential support for the IDH suggesting that intermediate levels of physical disturbance intensity influence the structure and functioning of termite assemblages in semi-arid savanna.