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.     

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.     

Why is the number of primary tunnels of the formosan subterranean termite,Coptotermes formosanus Shiraki (Isoptera: Rhinotermidae), restricted during foraging?

Subterranean termites forage by digging a network of tunnels to come into contact with food sources. When 1000 termites (Coptotermes formosanus Shiraki) were placed in a laboratory arena, 6.7 primary tunnels were constructed. The aim of this study was to explain the empirical observation in which termites restrict the number of primary tunnels. To this end, we constructed a model to simulate termite tunnel patterns based on empirical data and to calculate food transportation efficiency, γ, for the tunnel patterns. The efficiency was defined as the ratio of the number of encountered food particles to the sum of the shortest length from the location of encountered food particles to the initial position of growth of the tunnel. The γ was maximized when the number of primary tunnels was 5 or 6, which was fairly consistent with the empirical number of primary tunnels. This result indicated that termites may restrict the number of their primary tunnels to improve the transportation efficiency, which is directly related to their survival.     

Food encounter rates of simulated termite tunnels with variable food size/distribution pattern and tunnel branch length

Subterranean termites excavate tunnels in a search pattern to encounter food in soil. To investigate the effect of food size, food distribution and the branch length of tunnels on food encounter rate we used a lattice gas model to simulate tunnels of the Formosan subterranean termite, Coptotermes formosanus Shiraki. The model made use of minimized local rules derived from empirical data to simulate termite tunnel patterns in featureless soil. Food distributions with three types (uniform, random, and clumped) were defined by using an I-index proposed by Zimmer and Johnson (1985). The food encounter rate was higher in a clumped than in non-clumped (uniform and random) distribution of food particles. When food particle size was varied in random distributions of food particles a maximum encounter rate was found, with particles of larger or smaller size being encountered less frequently. We also discussed the relationship between the branch tunnel length and the tunnel search pattern in minimizing the redundancy of overlapping branches.     

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.     

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.     

Movement efficiency and behavior of termites in tunnels with changing width

Subterranean termites build extensive underground galleries that consist of elaborate tunnels and channels to forage for food resources. The changes in tunnel width along the length of the tunnel are related to both biotic (e.g., termite activity) and abiotic factors (e.g., soil density). Termites transport food through the tunnels from food sources to their nest. Thus, understanding the relationship between traveling behavior in the tunnels and changing width is important to comprehend the stability of the termite ecosystem. In the present study, we explored the traveling behavior of termites in terms of movement efficiency, where the movement efficiency was defined as the time (τ) needed for a termite to pass through a tunnel. To do so, we designed artificial tunnels with linearly changing width in a two-dimensional arena. The tunnel widths, W ₁ (for the entrance) and W ₂ (for the exit), were 2, 3, 4, 5, and 6 mm. We systematically observed the traveling behavior of the termites Reticulitermes speratus kyushuensis Morimoto (Isoptera: Rhinotermitidae) in the artificial tunnels and measured τ. The value of τ increased with the increase of W ₂, regardless of W ₁. τ was longer in the case of W ₁ < W ₂ than that of W ₁ > W ₂. The experimental results can be explained by behavioral differences observed in each case. The implications of the findings are briefly discussed in relation to termite foraging efficiency and the development of individual-based models for the construction of termite tunnels.     

Analysis of the responses of termites to tunnel irregularity

Subterranean termites build extensive underground galleries consisting of elaborate tunnels and channels to forage food resources. Diverse soil conditions surrounding the tunnels, such as soil density, may cause irregularities in the size and shape of the tunnels, and termites are likely to encounter a number of tunnel irregularities while traveling. Considering the tunnel length, how termites respond to an irregularity is likely to affect their movement efficiency, and this in turn is directly correlated to their foraging efficiency. To understand the response of termites, we designed an artificial linear tunnel with rectangular irregularities in a 2-D arena. The tunnel widths, W, were 3 and 4?mm. The rectangular irregularities were 2?mm in width and of varying heights H (2, 1, 0, ?1, and ?2?mm). The positive and negative sign of H represents a convex and concave structure, respectively. We systematically observed the movement of termites, Coptotermes formosanus Shiraki, at the irregularity and quantified the time needed, τ, for a termite to pass the irregularity. The time τ was shorter for (W, H)?=?(3, 0) and (3, ?1) than for (W, H)?=?(3, 1), (3, 2), and (3, ?2). The time τ was longer for (W, H)?=?(4, ?1), and (4, ?2), than for (W, H)?=?(4, 0), (4, 1) and (4, 2). Four types of behaviors explained the response to the irregularity. The implications of these findings are briefly discussed in relation to termite foraging efficiency.     

Fungal nutrition allocation enhances mutualism with fungus-growing termite

Fungal nodules and aged fungus gardens are products of termite fungiculture systems, and are the diets of termites. To understand the nutrition flow in fungiculture, we quantified the number and mass of fungal nodules produced along with fungus garden maturation and analysed the α-amino acid and fatty acid compositions of fungal nodules, fungus gardens, and termite tissues of a fungus-growing termite, Odontotermes formosanus. 1 g of fungus garden produced 5,148 fungal nodules (∼68.0 mg). Approximately 7.0% of α-amino acids were allocated to the fungal nodules and the rest (∼93.0%) remained in the fungus gardens. The compositions of α-amino acids or fatty acids in aged fungus gardens and fungal nodules were more similar to that of termite tissues than fresh fungus gardens, which supports the idea that termites nutritionally depend on the fungal products. Among the 18 α-amino acids, tryptophan was an essential amino acid and was the only one missing from fresh and aged fungus gardens, but found in fungal nodules at significantly higher concentrations. Hence, termites must consume fungal nodules to obtain tryptophan for survival. Furthermore, the fungus spores incorporated in nodules, were transferred when nodules were ingested by termites. We propose that allocating tryptophan in fungal nodules is crucial to enhance the mutualism between the fungus and termite.     

Phylogenetic diversity and physiology of termite gut spirochetes

The hindgut microbiota of termites includes an abundant andmorphologically diverse population of spirochetes. However,our understanding of these symbionts has remained meager sincetheir first observation in termite guts by Leidy over a centuryago, in part because none had ever been isolated in culture.Recently, this situation has changed dramatically with the applicationof cultivation-independent molecular methods to determine theirphylogeny, and with the isolation of the first pure cultures.The emerging picture is that earth's termites constitute anenormous reservoir of novel spirochetes, which possess metabolicproperties (H₂/CO₂-acetogenesis and N₂ fixation) hitherto unrecognizedin spirochetes and which contribute to the carbon, nitrogenand energy requirements of their termite host. These discoverieshelp to explain the enigmatic dominance of CO₂-reductive acetogenesisover methanogenesis in the hindgut of many termites, as wellas the old observation that elimination of spirochetes fromthe gut results in decreased termite survival.     

Can interaction specificity in the fungus-farming termite symbiosis be explained by nutritional requirements of the fungal crop?

Fungus-growing termites are associated with genus-specific fungal symbionts, which they acquire via horizontal transmission. Selection of specific symbionts may be explained by the provisioning of specific, optimal cultivar growth substrates by termite farmers. We tested whether differences in in vitro performance of Termitomyces cultivars from nests of three termite species on various substrates are correlated with the interaction specificity of their hosts. We performed single-factor growth assays (varying carbon sources), and a two-factor geometric framework experiment (simultaneously varying carbohydrate and protein availability). Although we did not find qualitative differences between Termitomyces strains in carbon-source use, there were quantitative differences, which we analysed using principal component analysis. This showed that growth of Termitomyces on different carbon sources was correlated with termite host genus, rather than host species, while growth on different ratios and concentrations of protein and carbohydrate was correlated with termite host species. Our findings corroborate the interaction specificity between fungus-growing termites and Termitomyces cultivars and indicate that specificity between termite hosts and fungi is reflected both nutritionally and physiologically. However, it remains to be demonstrated whether those differences contribute to selection of specific fungal cultivars by termites at the onset of colony foundation.     

Measurement of the time required for termites to pass each other in tunnels of different curvatures

Subterranean termites construct complex tunnel networks for foraging. During travel in the tunnels, termites often encounter one another when passing in opposite directions. Such encounters are likely to affect the “movement efficiency,” which is the time required for a termite to travel a certain distance in a tunnel. In this study, we explored how individual–individual encounters affect movement efficiency in tunnels by measuring the time (τ) taken by two termites to pass one another in tunnels of different curvatures. Artificial tunnels of 5 cm in length and variable widths (W) of 2, 3, or 4 mm were made. Tunnel distance (D) was 2, 3, 4, or 5 cm. When D had a higher value, curvature was lower. When W = 2, τ was significantly shorter in the tunnel with D = 5 than in tunnels of D = 2, 3, or 4, whereas τ was statistically the same for D = 2, 3 and 4. When W = 3, τ was shorter in the tunnel with D = 5 than for D = 3 and 4, while τ was longer in the tunnel with D = 2 than for D = 3 and 4. When W = 4, τ was longer in the tunnels with D = 2 and 3 than for D = 4 and 5. Based on these observations, 3 types of termite behavior were identified: biased walking, backward walking, and zigzag walking. We considered these results in relation to foraging efficiency.     

Tunnel formation by Reticulitermes flavipes and Coptotermes formosanus (Isoptera: Rhinotermitidae) in response to wood in sand.

The tunneling responses of two subterranean termite species, Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar), to the presence of sound wood in laboratory arenas were studied. Branching pattern and the speed of tunnel construction between R. flavipes and C. formosanus also were compared. Patlak's residence index (rho) was generated using the length, width, speed of construction, and area of the primary tunnels built by termites. In the same allotted time, C. formosanus built wider and shorter primary tunnels, whereas R. flavipes built thinner and longer primary tunnels. The presence of wood did not affect termite tunnel formation. This lack of variation in tunnel formation parameters was evidenced by the inability of the termites to locate wood sources over distance, even as short as 2.5 mm, and by the similar tunneling behaviors in areas of the arena with or without wood. Patlak's model predicted the densities of tunnels with an error between 9 and 28%. in experiments with R. flavipes exposed to a range of 0-8,000 g of wood, and between 61 and 87% in experiments with C. formosanus. These results indicated that the residence index can provide a qualitative measure of the effect of habitat heterogeneity on the individual termite tunnels. The tunneling constructions strategy of these subterranean termites is discussed.     

Directional selection by the subterranean termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) at tunnel intersections

Subterranean termites construct complicated tunnel networks for foraging below ground. Thus, they often encounter tunnel intersections during foraging activity. Directional selection by termites at intersections is likely to affect foraging efficiency because depending on their selection, the path length from food resources to the nest can vary significantly. In order to understand how termites are guided to choose the most economical path without the use of pheromones, we artificially excavated two tunnels of varying widths (W₁ and W₂; 2, 3, or 4 mm) that intersected at a 90° angle in each of nine soil‐filled arenas. We observed the directional selection of termites at intersections in arenas with combinations of W₁ (mm) and W₂ (mm) (W₁, W₂). For (W₁, W₂) = (2, 2) and (4, 4), termites statistically equally chose the three directions left, right, and straight, while for the (3, 3) arena combination, termites preferentially decided to go straight. On the other hand, for (W₁, W₂) = (2, 3) (2, 4), and (3, 4), termites advancing from narrower tunnels into intersections tended to turn right or left, while termites coming from the wider tunnel were more inclined to go straight. On the assumption that a wider tunnel is more frequently used by termites in the field, we can deduce that the wider tunnel may represent the most efficient/shortest path. Thus, this simple selection mechanism can prevent termites from deviating from the most economical path.     

Dependence of the higher termite, Nasutitermes exitiosus and the lower termite, Coptotermes lacteus on their gut flora

The importance of the gut microorganisms in the termites Nasutitermes exitiosus and Coptotermes lacteus was investigated by feeding them with antibiotics. With N. exitiosus, antibiotics which killed both the bacteria and the spirochaetes (ampicillin, kanamycin, chloramphenicol, erythromycin, cephaloridine, tetracycline) reduced the life span of the termite from 250 days to about 13 days, whereas antibiotics which had little effect on the flora (penicillin, methicillin) did not greatly reduce the life span of the termite. The essential role of the spirochaetes in N. exitiosus was shown by feeding metronidazole, or exposing the termites to pure oxygen. Both treatments killed the spirochaetes, but not the bacteria, resulting in a life span for the termite of 13–22 days. Acid fuchsin did not kill the spirochaetes. Fungi were not essential for N. exitiosus. In C. lacteus all treatments, except that with acid fuchsin, killed the protozoa, thereby reducing the life span of the termite from 69 days to 6–29 days.     

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.     

The role of logistic constraints in termite construction of chambers and tunnels

In previous models of the building behaviour of termites, physical and logistic constraints that limit the movement of termites and pheromones have been neglected. Here, we present an individual-based model of termite construction that includes idealized constraints on the diffusion of pheromones, the movement of termites, and the integrity of the architecture that they construct. The model allows us to explore the extent to which the results of previous idealized models (typically realised in one or two dimensions via a set of coupled partial differential equations) generalize to a physical, 3-D environment. Moreover we are able to investigate new processes and architectures that rely upon these features. We explore the role of stigmergic recruitment in pillar formation, wall building, and the construction of royal chambers, tunnels and intersections. In addition, for the first time, we demonstrate the way in which the physicality of partially built structures can help termites to achieve efficient tunnel structures and to establish and maintain entrances in royal chambers. As such we show that, in at least some cases, logistic constraints can be important or even necessary in order for termites to achieve efficient, effective constructions.     

Optimal length distribution of termite tunnel branches for efficient food search and resource transportation

Subterranean termites excavate branching tunnels for searching and transporting food in soil. Experimentally, the length distribution of the branch tunnels, P(L), was characterized by the exponentially decaying function, P(L)  exp(−L) with a branch length exponent of  = 0.15. To evaluate the significance of this value, we used a lattice model to simulate tunnels of the Formosan subterranean termite, Coptotermes formosanus Shiraki in featureless soil and computed the ratio of energy gain for obtained food to loss for transporting food for a given time, γ for various simulated tunnel patterns with the different values of . In simulation, the γ was maximized at 0.15 <  < 0.20 for the number of primary tunnels N = 6, 8, and 10. Our results indicate that tunnels with branch length distributions similar to those derived from empirical tunnel patterns result in tunnels made up of highly efficient paths to search and transport resources.     

Tunnel geometry of the subterranean termite Reticulitermes grassei （Isoptera： Rhinotermitidae）in response to sand bulk density and the presence of food

The cryptic habits of subterranean termites restricts detailed analysis of their foraging patterns in situ, but the process is evidently dominated by tunnel constructions connecting the nest with woody resources discovered within the territory of each colony. In this study, tunnel formation and orientation were studied experimentally in the termite Reticulitermes grassei （Clement）, using 2-dimensional laboratory foraging arenas con- taining fine sand as the substratum. The building of exploratory tunnels over a 10-day period and the geometry of the resulting network are described. Fractal analysis showed that tunnel geometry had a fractal dimension, regardless of the total length tunnelled whether foragers encountered the food source or not. The bulk density of the sand in the arenas affected the distances tunnelled, with higher density reducing construction, but did not affect tunnel geometry. Tunnels were not discernibly orientated with respect to the positioning of the food source, even in a situation where termites had failed to find the food source at a distance of less than 50 mm, suggesting that volatiles from wood are not attractants.     

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.