A novel approach to characterize branching network: Application to termite tunnel patterns

We defined a novel “branch length similarity” (BLS) entropy, S, on a simple network consisting of a single node and branches. This simple network is referred to as “unit branching network” (UBN) because UBNs are components of larger networks. As an application of BLS entropy, we considered the characterization of termite tunnel patterns because termite tunnel patterns can be broken down into a collection of simple units consisting of a single node and branches. These simple units correspond to UBNs. To this end, in additional to the entropy, we introduced the standard deviation (σ) of the difference in S between UBNs connected by a single tunnel branch. Forty simulated tunnel patterns were created for each of two termite species, Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki. These patterns were projected into <S>–σ phase space in order to assess their topological properties. This approach showed that for R. flavipes, their coordinates were relatively more clustered than those of C. formosanus. This result reflected that these two species were differently constrained by emergent property resulting from simple worker's tunneling behavior. We believe that the approach proposed in this study can be a useful tool to explore termite tunnel systems, but not limited to termite system.     

A mathematical model for the territorial competition of the subterranean termites Coptotermes formosanus and Reticulitermes flavipes (Isoptera: Rhinotermitidae)

The foraging territories of two subterranean termites, Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar), were simulated using a two-dimensional model to explore how territorial competition changes according to two variables characterizing territory formation: the total number of territories, and the blocking probability. Meanwhile, the blocking probability quantitatively describes the likelihood that a tunnel will be terminated when another tunnel is encountered. In our previous study, we introduced an interference coefficient γ to characterize territorial competition, and obtained γ as a function of the total number of territories and the blocking probability for a single termite species by model simulation. In the field, the territorial competition of more than two termite species is frequently observed. Here, we extended the γ function to be able to explain the competition between the two species by applying statistical regression to the simulation data. Further, we statistically checked the extended γ function by comparing the γ function for a single species. We also discuss another approach to mathematically derive the extended γ function, which can be easily generalized for use in cases of territorial competition involving more than two termite species.     

Volatile Fatty Acid Production by the Hindgut Microbiota of Xylophagous Termites

Acetate dominated the extracellular pool of volatile fatty acids (VFAs) in the hindgut fluid of Reticulitermes flavipes, Zootermopsis angusticollis, and Incisitermes schwarzi, where it occurred at concentrations of 57.9 to 80.6 mM and accounted for 94 to 98 mol% of all VFAs. Small amounts of C₃ to C₅ VFAs were also observed. Acetate was also the major VFA in hindgut homogenates of Schedorhinotermes lamanianus, Prorhinotermes simplex, Coptotermes formosanus, and Nasutitermes corniger. Estimates of in situ acetogenesis by the hindgut microbiota of R. flavipes (20.2 to 43.3 nmol · termite⁻¹ · h⁻¹) revealed that this activity could support 77 to 100% of the respiratory requirements of the termite (51.6 to 63.6 nmol of O₂ · termite⁻¹ · h⁻¹). This conclusion was buttressed by the demonstration of acetate in R. flavipes hemolymph (at 9.0 to 11.6 mM), but not in feces, and by the ability of termite tissues to readily oxidize acetate to CO₂. About 85% of the acetate produced by the hindgut microbiota was derived from cellulose C; the remainder was derived from hemicellulose C. Selective removal of major groups of microbes from the hindgut of R. flavipes indicated that protozoa were primarily responsible for acetogenesis but that bacteria also functioned in this capacity. H₂ and CH₄ were evolved by R. flavipes (usually about 0.4 nmol · termite⁻¹ · h⁻¹), but these compounds represented a minor fate of electrons derived from wood dissimilation within R. flavipes. A working model is proposed for symbiotic wood polysaccharide degradation in R. flavipes, and the possible roles of individual gut microbes, including CO₂-reducing acetogenic bacteria, are discussed.     

Simulation study on the tunnel networks of subterranean termites and the foraging behavior

Most subterranean termites forage for food by creating tunnel galleries underground. These tunnel networks reflect a compromise between foraging efficiency and other environmental constraints, such as soil hardness and moisture content. Thus, understanding tunnel networks is important for understanding foraging behavior. Due to the difficulties in direct observation of tunneling patterns in the field, we used a theoretical approach for this analysis. We first constructed a lattice model to simulate the tunnel networks of Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar) on the basis of the experimental data provided by Su et al. (Su, N.-Y., Stith, B.M., Puche, H., Bardunias, P., 2004. Characterization of tunneling geometry of subterranean termites (Isoptera: Rhinotermitidae) by computer simulation. Sociobiology 44 (3), 471–483.). Using this model and two of its modified versions, we explored the relationship between the food encounter rate and food distributions and analyzed how this relationship is influenced by changes in the tunnel characteristic constituents, such as the branching tunnel length and frequency. Additionally, we investigated the effects of landscape heterogeneity on the foraging efficiency. In the discussion, we briefly introduced our novel individual-based model comprising individual termites and their surroundings, and we addressed the necessity of this model in the functioning of the network and the formation of the network in relation to foraging behavior.     

Antitermitic effect of the Lantana camara plant on subterranean termites (Isoptera: Rhinotermitidae)

Abstract The insecticidal effects of Lantana camara L. (flowers, leaves, stems and roots) and the soil where lantana had been growing, on foraging activity and survival of the subterranean termites Coptotermes formosanus and Reticulitermes flavipes were examined in a 3-week experiment. The soil in which lantana had been growing had no effect on termite tunneling and survival. Incorporation of chipped fresh lantana leaves and stems into soil had no effect on mortality but caused significant reduction in tunneling. The 5-cm wide barrier of soil with lantana tissue incorporated effectively repelled groups of both species from penetrating the barrier and thus prevented infestation of a piece of wood on the other side of the barrier. C. formosanus was more sensitive in avoiding the barrier than R. flavipes. Leaves, stems and flowers were more repellent than roots. These results provide preliminary evidence that fresh-cut lantana leaves, stems and flowers may have use as additives to garden mulches against termites.     

Behavioral Response of Two Subterranean Termites (Isoptera: Rhinotermitidae) to Vibrational Stimuli

Behavioral responses to vibrational stimuli were examined in two subterranean termite species, Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar). Termites habituated to vibrational stimulation when in social groups, but failed to do so individually, indicating that habituation is a collective action. In assays on termite groups, both species demonstrated a similar pattern of behavioral responses to vibrational stimuli: evanescent cessation of activity and movement, followed by withdrawal from the vibration source. Groups of both species then gradually moved back toward the vibration source as a consequence of continuous exposure. However, it took a significantly shorter period for C. formosanus to return (57 s) to the test arena and to resume (80 s) normal foraging activities in the test arena compared with R. flavipes, which took 97 and 227 s, respectively, when exposed to the vibration frequency of 120 bmpm. High vibration frequency (240 bmpm) increased the time required to return (C. formosanus, 80 s; R. flavipes, 153 s) and to resume regular locomotion (C. formosanus, 186 s; R. flavipes, 263 s). Our experiments demonstrate that workers play a crucial part in adjusting groups of termites to distressful vibrations. Soldiers of R. flavipes demonstrated similar behavioral responses as workers, however, C. formosanus soldiers exhibited a transient positive response before withdrawal. An erratum to this article is available at .     

Characterization of a laccase from a wood‐feeding termite,Coptotermes formosanus

Coptotermes formosanus Shiraki is a wood‐feeding termite which secretes a series of lignolytic and cellulolytic enzymes for woody biomass degradation. However, the lignin modification mechanism in the termite is largely elusive, and the characteristics of most lignolytic enzymes in termites remain unknown. In this study, a laccase gene lac1 from C. formosanus was heterogeneously expressed in insect Sf9 cells. The purified Lac1 showed strong activities toward hydroquinone (305 mU/mg) and 2,6‐dimethoxyphenol (2.9 mU/mg) with low K_m values, but not veratryl alcohol or 2,2’‐azino‐bis (3‐ethylbenzothiazoline‐6‐sulfonic acid). Lac1 could function well from pH 4.5 to 7.5, and its activity was significantly inhibited by H₂O₂ at above 4.85 mmol/L (P < 0.01). In addition, the lac1 gene was found to be mainly expressed in the salivary glands and foregut of C. formosanus, and seldom in the midgut or hindgut. These findings suggested that Lac1 is a phenol‐oxidizing laccase like RflacA and RflacB from termite Reticulitermes flavipes, except that Lac1 was found to be more efficient in phenol oxidation, and it did not require H₂O₂ for its function. It is suspected that this kind of termite laccase might only be able to directly oxidize low redox‐potential substrates, and the high redox‐potential groups in lignin might be oxidized by other enzymes in the termite or by using the Fenton reaction.     

Effect of landscape heterogeneity on termite tunnel pattern: Simulation study

Although the environment in which termites live is very heterogeneous, most experimental studies on the termite tunnel patterns have been conducted on homogeneous sand substrates. In order to explore how the heterogeneity affects tunnel patterns, I developed an agent-based model to simulate termite tunneling behavior at the individual level. In this model, grid space consists of easy and difficult areas for tunneling. Heterogeneity, H, was defined as the degree of the mixture of the two areas. The tunnel patterns formed by changing the number of termites, N, and H were quantitatively characterized by territory circularity and the territory area. These patterns were categorized into two groups, one with a small territory area and high circularity (group 1) and the other with a large area and low circularity (group 2). Considering the previous study that the termite populations with high N values have high territorial scalability, it can be said that the territories belonging to group 2 have higher foraging abilities and viability than those belonging to group 1. The simulation results showed that the tunnel patterns generated for small N and high H belonged to group 2. This implies that the heterogeneity can make a positive contribution to the expansion of the foraging area by effectively focusing the foraging energy of a termite population. I briefly discussed the mechanism of this positive role and the limitations of this simulation study. In addition, I discussed issues that need to be resolved in the near future to overcome the limitations.     

The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: Implications for the evolution of the worker and pseudergate castes, and foraging behaviors

A phylogenetic hypothesis of termite relationships was inferred from DNA sequence data. Seven gene fragments (12S rDNA, 16S rDNA, 18S rDNA, 28S rDNA, cytochrome oxidase I, cytochrome oxidase II and cytochrome b) were sequenced for 40 termite exemplars, representing all termite families and 14 outgroups. Termites were found to be monophyletic with Mastotermes darwiniensis (Mastotermitidae) as sister group to the remainder of the termites. In this remainder, the family Kalotermitidae was sister group to other families. The families Kalotermitidae, Hodotermitidae and Termitidae were retrieved as monophyletic whereas the Termopsidae and Rhinotermitidae appeared paraphyletic. All of these results were very stable and supported with high bootstrap and Bremer values. The evolution of worker caste and foraging behavior were discussed according to the phylogenetic hypothesis. Our analyses suggested that both true workers and pseudergates (“false workers”) were the result of at least two different origins. Our data support a traditional hypothesis of foraging behavior, in which the evolutionary transition from a one-piece type to a separate life type occurred through an intermediate behavioral form.     

Hydrogen emission by three wood-feeding subterranean termite species (Isoptera: Rhinotermitidae): Production and characteristics

Abstract Hydrogen emission by wood-feeding termites, Coptotermes formosanus, Reticulitermes flavipes and Reticulitermes virginicus, was investigated upon a cellulosic substrate as their food source. The emission rates among the three species tested were significantly different and R. virginicus demonstrated the greatest H₂ emission at 4.78 ± 0.15 μmol/h/g body weight. In a sealed test apparatus, H₂ emission for each termite species showed a quick increase at the initial incubation hours (3–6 h), followed by a slower growth, possibly due to the feedback inhibition by gas accumulation. Further investigation revealed that continuous H₂ emission could be maintained by reducing the H₂ partial pressure in the sealed container. The bioconversion of cellulose to molecular H₂ by the subterranean termites tested could reach as high as 3 858 ± 294 μmol/g cellulose, suggesting that the termite gut system is unique and efficient in H₂ conversion from cellulosic substrate.     

Exploring landscape structure effect on termite territory size using a model approach

The foraging territory of the Formosan subterranean termite, Coptotermes formosanus Shiraki, was simulated by using a lattice model in order to study how landscape structure affects the foraging territory. Three kinds of landscape were generated on lattice space: ideal, random and fractal landscape. Each lattice cell had a value ranging from 0.0 to 1.0, interpreted as transition probability, P_trans, which represents spatially distributed property of the landscapes. The heterogeneity of the fractal landscape was characterized by a parameter, H, controlling aggregation of lattice cells with higher value of P_trans. Higher H values corresponded to higher aggregation levels. The model made use of minimized local rules based on empirical data that determines the development of the foraging territory. Additionally, seasonal cycle (summer and winter season), and obstacles which hinder the growth of the territory were incorporated in the model as environmental variables. Territory size was largest in the ideal landscape while it was larger in the random landscape than in the fractal landscape. As obstacle density increased, the territory size decreased. In the fractal landscape, the territory size increased, decreased, and increased again as H increased.     

Effects of concentration,distance, and application methods of Altriset (Chlorantraniliprole) on eastern subterranean termite (Isoptera: Rhinotermitidae)

The effects of various concentrations, distance, and application methods of Altriset (Chlorantraniliprole) were investigated against one of the most destructive termites, the eastern subterranean termite, Reticulitermes flavipes Kollar. Three laboratory experiments were conducted. First, we examined the concentration effect of treating the soil contiguously to established foraging tunnels at a fixed 1 m distance. The results demonstrated 100% termite control in 19 d posttreatment at 100 and 50 μg/g and 27% termite mortality at 25 μg/g. Second, we tested the distance effect of the soil treatment (2 and 4 m) on the efficacy of Altriset to the satellite termite populations at a fixed 50 μg/g concentration. This resulted in 100% termite control in 22 d posttreatment at both 2 and 4 m. Third, we examined the effect of differing application methods using 12.5 and 25 μg/g prior to the establishment of foraging tunnels at a fixed 1m distance. This illustrated 100% termite control in 9 d posttreatment at 25 μg/g and 12 d posttreatment at 12.5 μg/g. The third experiment demonstrated soil treatments that were applied prior to termite tunnel establishment had greater efficacy than applications made post tunnel construction. Our results provide a comprehensive understanding about the efficacy of Altriset treatments on eastern subterranean termites.     

Minimizing moving distance in deposition behavior of the subterranean termite

Subterranean termite nests are located underground and termites forage out by constructing tunnels to reach food resources, and tunneling behavior is critical in order to maximize the foraging efficiency. Excavation, transportation, and deposition behavior are involved in the tunneling, and termites have to move back and forth to do this. Although there are three sequential behaviors, excavation has been the focus of most previous studies. In this study, we investigated the deposition behavior of the Formosan subterranean termite, Coptotermes formosanus Shiraki, in experimental arenas having different widths (2, 3, and 4 mm), and characterized the function of deposited particles. We also simulated moving distance of the termites in different functions. Our results showed that total amounts of deposited particles were significantly higher in broad (4 mm width) than narrow (2 mm) tunnels and most deposited particles were observed near the tip of the tunnel regardless of tunnel widths. In addition, we found that deposited particles followed a quadratic decrease function, and simulation results showed that moving distance of termites in this function was the shortest. The quadratic decrease function of deposited particles in both experiment and simulation suggested that short moving distance in the decrease quadratic function is a strategy to minimize moving distance during the deposition behavior.     

IDH knockdown alters foraging behavior in the termite Odontotermes formosanus in different social contexts

Foraging, as an energy-consuming behavior, is very important for colony survival in termites. How energy metabolism related to glucose decomposition and adenosine triphosphate (ATP) production influences foraging behavior in termites is still unclear. Here, we analyzed the change in energy metabolism in the whole organism and brain after silencing the key metabolic gene isocitrate dehydrogenase (IDH) and then investigated its impact on foraging behavior in the subterranean termite Odontotermes formosanus in different social contexts. The IDH gene exhibited higher expression in the abdomen and head of O. formosanus. The knockdown of IDH resulted in metabolic disorders in the whole organism. The dsIDH-injected workers showed significantly reduced walking activity but increased foraging success. Interestingly, IDH knockdown altered brain energy metabolism, resulting in a decline in ATP levels and an increase in IDH activity. Additionally, the social context affected brain energy metabolism and, thus, altered foraging behavior in O. formosanus. We found that the presence of predator ants increased the negative influence on the foraging behavior of dsIDH-injected workers, including a decrease in foraging success. However, an increase in the number of nestmate soldiers could provide social buffering to relieve the adverse effect of predator ants on worker foraging behavior. Our orthogonal experiments further verified that the role of the IDH gene as an inherent factor was dominant in manipulating termite foraging behavior compared with external social contexts, suggesting that energy metabolism, especially brain energy metabolism, plays a crucial role in regulating termite foraging behavior.     

Interspecific Interactions Between Coptotermes formosanus and Reticulitermes flavipes (Isoptera: Rhinotermitidae) in Laboratory Bioassays

Experiments were conducted to examine competitive interactions between the Formosan subterranean termite, Coptotermes formosanus Shiraki (FST), and the eastern subterranean termite, Reticulitermes flavipes (Kollar) (EST), using groups of termites with different worker:soldier proportions. Experiments were conducted using three connected test chambers: an FST chamber, an unoccupied center chamber, and an EST chamber. When groups of FST were comprised of 20% soldiers versus 2% EST soldiers, only 8% of center chambers were occupied exclusively by EST. When groups of FST were comprised of 10% soldiers versus 1% EST soldiers, 44% of center chambers were occupied exclusively by EST. When the only food source was located in the center chamber, 60% of center chambers were occupied by both species. FST did not completely displace EST in any of these experiments.     

Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts

A morphologically distinct, filamentous methanogen was isolated from hindguts of the subterranean termite, Reticulitermes flavipes (Kollar) (Rhinotermitidae), wherein it was part of the microbiota colonizing the hindgut wall. Individual filaments of strain RFM-3 were 0.23–0.28 μm in diameter and usually > 50 μm in length and aggregated into flocs that were often ≥ 0.1 mm in diameter. Optimal growth of strain RFM-3 was obtained at pH 7.0–7.2 and 30° C with a yeast-extract-supplemented, dithiothreitol-reduced medium in which cells produced stoichiometric amounts of methane from H₂ + CO₂. The morphology and gram-positive staining reaction of strain RFM-3, as well as its resistance to cell lysis by various chemical agents and its restriction to H₂ + CO₂ as an energy source, suggested that it was a member of the Methanobacteriaceae. The nucleotide sequence of the SSU-rRNA-encoding gene of strain RFM-3 confirmed this affiliation and also supported its recognition as a new species of Methanobrevibacter, for which the epithet filiformis is herewith proposed. Although M. filiformis was one of the dominant methanogens in R. flavipes collected from Woods Hole (Mass., USA), cells of similar morphology were not consistently observed in R. flavipes collected from different geographical locations. Received: 15 September 1997 / Accepted: 20 November 1997     

Effects of tunnel structures of two termite species on territorial competition and territory size

The foraging territories of 2 subterranean termites, Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar), were simulated using a model to explore how territorial intraspecific competition changes with 4 variables characterizing the formation of territory: the number of primary tunnels, N₀; the branching probability, P_branch; the number of territories, N; and the blocking probability, P_block. The blocking probability P_block quantitatively describes the probability that a tunnel will be terminated when another tunnel is encountered; higher P_block values indicate more likely termination. Higher tunnel-tunnel encounters led to denser tunnel networks. We defined a territory as a convex polygon containing a tunnel pattern and explored the effects of competition among termite colonies on territory size distribution at steady state attained after sufficient simulation time. At the beginning of the simulation, N = 10, 20,…, 100 initial territory seeds were randomly distributed within a square area. In our previous study, we introduced an interference coefficient γ to characterize territorial competition. Higher γ values imply higher limitations on network growth. We theoretically derived γ as a function of P_block and N. In this study, we considered the constants in γ as functions of N₀ and P_branch so as to quantitatively examine the effect of tunnel structure on territorial competition. By applying statistical regression to the simulation data, we determined the generalized γ functions for both species. Under competitive conditions, territory size is most strongly affected by N₀, while the outcome of territorial competition is most strongly affected by N, followed by P_block and N₀.     

Behavioral Interactions Between <Emphasis Type="Italic">Aphaenogaster rudis</Emphasis> (Hymenoptera: Formicidae) and <Emphasis Type="Italic">Reticulitermes flavipes</Emphasis> (Isoptera: Rhinotermitidae): The Importance of Physical Barriers

Predation pressure from ants is a major driving force in the adaptive evolution of termite defense strategies and termites have evolved elaborate chemical and physical defenses to protect themselves against ants. We examined predator–prey interactions between the woodland ant, Aphaenogaster rudis (Emery) and the eastern subterranean termite, Reticulitermes flavipes (Kollar), two sympatric species widely distributed throughout deciduous forests in eastern North America. To examine the behavioral interactions between A. rudis and R. flavipes we used a series of laboratory behavioral assays and predation experiments where A. rudis and R. flavipes could interact individually or in groups. One-on-one aggression tests revealed that R. flavipes are vulnerable to predation by A. rudis when individual termite workers or soldiers are exposed to ant attacks in open dishes and 100% of termite workers and soldiers died, even though the soldiers were significantly more aggressive towards the ants. The results of predation experiments where larger ant and termite colony fragments interacted provide experimental evidence for the importance of physical barriers for termite colony defense. In experiments where the termites nested within artificial nests (sand-filled containers), A. rudis was aggressive at invading termite nests and inflicted 100% mortality on the termites. In contrast, termite mortality was comparable to controls when termite colonies nested in natural nests comprised of wood blocks. Our results highlight the importance of physical barriers in termite colony defense and suggest that under natural field conditions termites may be less susceptible to attacks by ants when they nest in solid wood, which may offer more structural protection than sand alone.