Mammalian predation on termites: tests with the burrowing mouse (Oxymycterus roberti) and its prey

Summary A laboratory study of mammalian predation on termites was conducted using the burrowing mouse (Oxymycterus roberti) and eight species of central Brazilian termites. The results of preference trials demonstrate that Oxymycterus discriminate between termite species and that the eight prey species fall into three groups: least preferred, most-preferred and a group of intermediate preference.Preferences of Oxymycterus are not explained by the size or the nutritional quality of the termite species. However, three measures of termite soldier-based defense do correlate highly with preference. Termite species with soldiers exhibiting a mechanical or mixed defense are greatly preferred by Oxymycterus over species with soldiers exhibiting a chemical based defense. This chemical defense by termites is effective in severely limiting predation by small mammals.     

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.     

Responses of Coptotermes formosanus and Reticulitermes flavipes (Isoptera: Rhinotermitidae) to three types of wood rot fungi cultured on different substrates

This study examined the responses of two termite species, the Formosan subterranean termite, Coptotermes formosanus Shiraki, and the eastern subterranean termite, Reticulitermes flavipes (Kollar), to three types of wood decay fungi: a brown rot fungus, Gloeophyllum trabeum (Persoon: Fries) Murrill; a white rot fungus, Phanerochaete chrysosporium Burdsall; and a litter rot fungus, Marasmiellus troyanus (Murrill) Singer. We also examined the responses of termites to these three types of fungi grown on different substrates. For all three fungal species, both termite species showed a strong preference for fungus-infected sawdust over uninfected sawdust. In choice tests, both termite species preferred sawdust infected with either M. troyanus or P. chrysosporium over G. trabeum. However, termites did not show any preference for fungus-infected potato dextrose agar over uninfected potato dextrose agar. Tunneling activity of C. formosanus was greater in sand treated with methanol extracts of fungus-infected sawdust than in sand treated with extracts of uninfected sawdust. Because chemicals in the fungal extracts caused termites to tunnel further into treated sand than untreated sand, these chemicals could potentially be used to direct termite foraging toward bait stations in the field.     

A comparison of two methods for sampling assemblages of subterranean,wood-eating termites (Isoptera)

Abstract Within a 50 × 50 m area of wandoo Eucalyptus capillosa woodland in the Western Australian wheatbelt, the diversity and frequency of occurrence of wood-eating termite species was assessed at two food types. Over a 12 month period, monthly termite activity was determined: (i) at sound/undecayed artificial baits (seasoned wooden stakes of Jarrah, Karri, Pine, Batu, Oregon; Jarrah sawdust; paper rolls); and (li) at naturally occurring timber, fallen logs and branches of wandoo, in varying stages of decay. Termite diversity was 11 species at baits, 18 species at wandoo out of an overall site richness of 21 species. Karri attracted the most species (9); sawdust attracted none. At wandoo, Nasutitermes exitiosus, Coptotermes acinaciformis and Occasitermes occasus accounted for 59% of samples where termites were recorded. At baits, Heterotermes occiduus accounted for a mean of 80% of samples across bait types, but was rarely sampled at wandoo (5% of samples). Only H. occiduus, C. acinaciformis and Amitermes neogermanus ate bait. Pine, Oregon and paper rolls were most effective in attracting foraging termites in terms of highest per cent of replicates showing bait consumption and highest consumption rates. Jarrah and Batu were least attractive to foraging termites. Samples from wandoo underestimated the relative frequency of occurrence of H. occiduus within the study site. Coptotermes acinaciformis, which attack large food items, and certain species of Amitermes, which forage on subterranean food, may have been underestimated by both sampling methods. These findings indicate that a proper understanding of the structure of wood-eating termite assemblages within a given area requires a composite sampling strategy which addresses termites that eat sound or decayed wood, as well as surface and subsurface foragers.     

Effect of a lignin-degrading fungus on feeding preferences of Formosan subterranean termite (Isoptera: Rhinotermitidae) for different commercial lumber

The feeding preferences of the Formosan subterranean termite, Coptotermes formosanus Shiraki, for commercial lumber Alaska yellow cedar, Chamaecyparis nootkatensis (D. Don) Spach; yellow birch, Betula alleghaniensis Britton; northern red oak, Quercus rubra L.; redwood, Sequoia sempervirers (D. Don) Endl; and spruce (Picea spp.) were examined to determine whether the presence of the lignin-degrading basidiomycete Marasmiellus troyanus (Murrill) Singer could alter the relative preference of termites for these wood species. In paired choice tests with fungus-inoculated sawdust versus control sawdust, termites showed a strong preference for the fungus-inoculated sawdust for all wood species tested, except for Alaska yellow cedar. In a multiple-choice test using sawdust without fungus, termites showed a very strong preference for red oak sawdust over the other three species. In a paired choice test using fungus-inoculated sawdust, termites showed a preference for redwood over red oak sawdust. In a feeding test using autoclaved wood blocks without fungal decay, there was no difference in termite consumption of birch, red oak, or redwood. The relative preference of termites for redwood increased when blocks were decayed by M. troyanus for 3 and 8 wk. These results indicate that chemical modifications due to fungal decay affected the feeding preference of termites for different commercial lumber.     

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.     

Fipronil enhanced natural occurrence of Fusarium solani (Hypocreales: Nectriaceae) on building infesting termite Heterotermes indicola Wasmann (Blattodea: Rhinotermitidae)

The Southeast Asian subterranean termite, Heterotermes indicola Wasmann (Blattodea; Rhinotermitidae), is recognized as a building infesting lower termite species in urban environment. The extensive use of chemical termiticides against aerial mud tubes and underground nests of H. indicola beneath the buildings could not suppress its infestation; however, it enhanced the environmental contamination and insecticide resistance. In the present study, we tried to control termites using naturally occurring entomopathogenic fungi Fusarium solani (Mart.) Sacc., along with sublethal concentrations of termiticide fipronil in no-choice feeding pathogenecity bioassay for 20?days. Termite mortality after 20?days of continuous exposure to highest fungal treatment 1?×?10⁹?conidia/mL was 10% exclusively, whereas 100% mortality was calculated just after 16?days of concurrently exposure to 5?ppm of fipronil and highest rate of fungus 1?×?10⁹?conidia/mL. These results indicated that insecticidal stress declined the immune response of termites and reduced the repellency of termites against fungal conidia by breaching the primary defense mechanism (allogrooming). This co-application of F. solani at suitable sublethal concentrations of fipronil showed the promising potential against termites that may reduce the selection pressure of pesticides and resistance risk by targeted pests, but further investigations are necessary for developing field trials.     

Assessment of the contamination and genotoxicity of soil irrigated with wastewater

Soil structures built by litter-feeding termites are one of the main soil translocation processes in dry tropical savanna. Runways (soil sheeting) made of soil particles cemented with salivary secretions covering the dead plant pieces collected on the ground surface represent the main soil structures. The aim of this study was to determine the impact of this soil engineering activity on the microbially-mediated N transformations (nitrification and denitrification) associated with termite sheeting. We investigated the hypothesis that the physicochemical and microbial properties of termite soil sheeting depend on (i) the termite species and (ii) the type of organic substrate consumed. Soil sheeting built by two of the main savanna species, Macrotermes subhyalinus and Odontotermes nilensis, were sampled on field plots treated with three different types of litter (Acacia leaves, millet straw, both whole and ground (< 500 µm), and cattle manure). The soils organic C, total N, inorganic N, microbial biomass, potential CO₂ respiration, nitrification and denitrification were measured. For both termite species and all types of litter, the soil sheeting was enriched in organic C and inorganic N, resulting in an increase in soil respiration, whereas the microbial biomass was unchanged with respect to the reference soil. With the exception of the soil nitrification potential, the type of organic substrate did not significantly affect the properties of the soil sheeting measured. However, the nitrogen cycle was affected differently by the two termite species. In O. nilensis sheeting, the denitrification potential was reduced with respect to the reference soil, whereas the nitrification potential was inhibited in M. subhyalinus sheeting. The changes in the nitrogen cycle processes resulted in an increase in NH₄₊ and NO_3– in the termite soil sheeting, increasing the availability of nitrogen to plants. This study reinforces the importance of termites as a keystone savanna group whose building activities have an effect on tropical soil mineralization.     

Studies on the Natural Durability of Tropical Timbers to termite attack

Small samples of 28 tropical timbers were tested with the dry-wood termite Cryptotermes cynocephalus and the subterranean termite Coptotermes curvignathus using several methods of testing. The results revealed that four among 28 species of wood were completely durable to the two species of termite. They are Dalbergia latifolia, Eusideroxylon zwageri, Intsia bijuga and Tectona grandis. Agathis alba, Dipterocarpus spp. and Mangifera spp. were classified as the most susceptible wood species to termites.     

Cryptic termites avoid predatory ants by eavesdropping on vibrational cues from their footsteps

Eavesdropping has evolved in many predator–prey relationships. Communication signals of social species may be particularly vulnerable to eavesdropping, such as pheromones produced by ants, which are predators of termites. Termites communicate mostly by way of substrate‐borne vibrations, which suggest they may be able to eavesdrop, using two possible mechanisms: ant chemicals or ant vibrations. We observed termites foraging within millimetres of ants in the field, suggesting the evolution of specialised detection behaviours. We found the termite Coptotermes acinaciformis detected their major predator, the ant Iridomyrmex purpureus, through thin wood using only vibrational cues from walking, and not chemical signals. Comparison of 16 termite and ant species found the ants‐walking signals were up to 100 times higher than those of termites. Eavesdropping on passive walking signals explains the predator detection and foraging behaviours in this ancient relationship, which may be applicable to many other predator–prey relationships.     

Parallel evolution of termite‐egg mimicry by sclerotium‐forming fungi in distant termite groups

Among the great diversity of insect–fungus associations, fungal mimicry of termite eggs is a particularly fascinating consequence of evolution. Along with their eggs, Reticulitermes termites often harbour sclerotia of the fungus Fibularhizoctonia sp., called ‘termite balls’, giving the fungus competitor‐free habitat within termite nests. The fungus has evolved sophisticated morphological and chemical camouflage to mimic termite eggs. To date, this striking insect–fungus association has been found in eight temperate termite species, but is restricted to the lower termite genera Reticulitermes and Coptotermes. Here, we report the discovery of a novel type of termite ball (‘Z‐type’) in the subtropical termite, Nasutitermes takasagoensis. Phylogenetic analysis indicated that the Z‐type termite ball is an undescribed Trechisporoid fungus, Trechispora sp., that is phylogenetically distant from Fibularhizoctonia, indicating two independent origins of termite‐egg mimicry in sclerotium‐forming fungi. Egg protection bioassays using dummy eggs revealed that Reticulitermes speratus and N. takasagoensis differ in egg‐size preference. A comparative study of termite ball size and egg‐size preference of host termites showed that both fungi evolved a termite ball size that optimized the acceptance of termite balls as a unit investment. Termite‐egg mimicry by these fungi offers a model case of parallel evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 531–537.     

Valuation of efficacy and nonrepellency of indoxacarb and fipronil-treated soil at various concentrations and thicknesses against two subterranean termites (Isoptera: Rhinotermitidae)

The efficacy and nonrepellency of indoxacarb (150 SC, 150 g [AI]/liter) and fipronil (Termidor SC, 9.1% [Al]) against field-collected eastern subterranean termite, Reticulitermes flavipes (Kollar), and the Formosan subterranean termite, Coptotermes formosanus Shiraki, were evaluated for mortality and penetration into treated soil in laboratory glass tube bioassays. Both insecticides were tested at five concentrations (0, 1, 10, 50, and 100 ppm) and two thicknesses (20 and 50 mm) of treated soil. Indoxacarb caused significantly greater mortality than controls at all treatment thicknesses of > or = 10 ppm, but not at 1 ppm. Concentration and treatment thickness of indoxacarb significantly affected termite mortality. Eastern subterranean termites were significantly more susceptible to indoxacarb than Formosan subterranean termites, but there were no intercolony differences in either species. Termites completely penetrated through all treatment thickness of indoxacarb-treated soil at all concentrations, except one of the six Formosan subterranean termite replicates of 50 mm at 50 ppm, when all termites were killed before tunneling through the treated soil. Fipronil resulted in significantly faster and greater termite mortality than indoxacarb at corresponding concentrations. Concentration and treatment thickness of fipronil also significantly affected termite mortality. There was no intercolony difference in susceptibility to either insecticide in either termite. Both termite species completely penetrated 20-mm treatments of all tested fipronil concentrations, as well as 50-mm soil treated with fipronil at < or = 10 ppm. At 50 and 100 ppm fipronil, termites tunneled only a mean of 87 +/- 0.21 and 47 +/- 0.18% deep into 50-mm treated soil, respectively, before death. Both insecticides demonstrated a delayed mode of activity and nonrepellency against the two termite species.     

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.     

Clay preference and particle transport behavior of Formosan subterranean termites （Isoptera： Rhinotermitidae）＂ A laboratory study

Although preference and utilization of clay have been studied in many higher termites, little attention has been paid to lower termites, especially subterranean termites. The Formosan subterranean termite, Coptotermes formosanus Shiraki, can modify its habitat by using clay to fill tree cavities. Here, the biological significance of clay on C. formosanus was investigated. Choice tests showed that significantly more termites aggre- gated in chambers where clay blocks were provided, regardless of colony group, observation period, or nutritional condition （fed or starved）. No-choice tests showed that clay had no observable effect on survivorship, live or dry biomass, water content, and tunneling activity after 33-35 d. However, clay appeared to significantly decrease filter paper consumption （dry weight loss）. Active particle （sand, paper, and clay） transport behavior was observed in both choice and no-choice tests. When present, clay was preferentially spread on the substrate, attached to the smooth surfaces of the containers, and used to line sand tunnels. Mechanisms and potential application of clay attraction are discussed.     

Abundance and diversity of termites (Isoptera) in imburnt versus burnt vegetation at the Barrens in Mediterranean Western Australia

Abstract Two years after an intense fire burnt large parts of the Barrens in Mediterranean Western Australia, its effects on wood-eating and litter-harvesting termites were investigated. Nine vegetation types varying in height, structure and floristics, were used for paired unburnt/burnt comparisons. Wood-eating termites were significantly less abundant and diverse in burnt stands, apparently by perishing in the fire rather than through food limitation. The harvester Tumulitermes westraliensis was not significantly affected by fire. Strategies enhancing persistence despite intense fire were construction of hard, protective clay mounds (Coptotermes frenchi, Amitermes obeuntis, T. westraliensis) and flexibility to site nests in diverse microhabitats, including the mounds of other termite species (Heterotermes).     

Use of Genetically Engineered Escherichia coli to Monitor Ingestion, Loss, and Transfer of Bacteria in Termites

Escherichia coli was transformed with a recombinant plasmid (pEGFP) containing the genes for ampicillin resistance and Green Fluorescent Protein (GFP). Escherichia coli expressing GFP (E. coli/GFP+) was then fed to workers of the termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). The transformed bacteria in the termite guts were detected by growing the gut flora under selective conditions and then checking the cultures for fluorescence. Recombinant plasmids in the termite gut were detected by plasmid extraction with subsequent restriction enzyme digest. The presence of the GFP gene in the gut of termites fed with E. coli/GFP+ was verified by PCR amplification. Transformed E. coli were ingested rapidly when workers fed on filter paper inoculated with E. coli/GFP+. After 1 day, 42% of termite guts harbored E. coli/GFP+. Transfer of E. coli/GFP+ from donor termites (fed with E. coli/GFP+) to recipients (fed with moist filter paper) occurred within 1 day. However, without continuous inoculation, termites lost the transformed bacteria within 1 week.     

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.     

Testing the role of cuticular hydrocarbons on intercolonial agonism in two subterranean termite species (Coptotermes) and their hybrids

Recognition of nestmates is an important function in many social insects, as it maintains colony integrity by preventing outsiders from entering the colony. Agonism usually results from the interaction of con-specific non-nestmate individuals in termite colonies. Previous studies hypothesized that the cuticular hydrocarbon (CHC) profile of individuals had a role in nestmate recognition. However, contradictory results from previous studies in some subterranean termites raise questions on the validity of the cuticular hydrocarbon hypothesis. In the current study, Coptotermes gestroi (Wasmann), Coptotermes formosanus Shiraki and their hybrids were reared in identical conditions from colony foundation. This approach eliminates sources of variability in their cuticular hydrocarbon profiles aside from a genetic component. The parental species displayed dissimilar profiles of predominant alkanes and methyl alkanes, but both hybrid types displayed an overlapping, intermediate profile of these CHC. The mixture of the most abundant CHCs alone did not determine kin recognition; while the two hybrid types’ CHC profiles converged, the hybrids still showed strong agonism. One of the hybrid mating types easily merged with C. formosanus, despite only partial genetic similarity and dissimilar cuticular profiles for the common alkanes and methyl alkanes. This study suggests that in Coptotermes termites, the variable abundance of the major alkanes and methyl alkanes commonly found in most Coptotermes species does not explain agonistic patterns, and that other factors such as possibly more complex but less abundant CHC are likely to be involved in colonial recognition.

     

Tunneling activity of subterranean termites (Isoptera: Rhinotermitidae) in sand with moisture gradients

Tunnel formation by Coptotermes formosanus and Reticulitermes flavipes was studied in a two-dimensional foraging arena with a moisture gradient. Moisture did not appear to affect tunneling when termite first emerged from the central release chamber. But as termites of both species moved further away from the chamber and into a moisture gradient, they tunneled significantly (P < 0.05) more in sand with a higher moisture content than in sand with a lower moisture content. Over the 10 d test period, both termite species tunneled more in sand with a higher moisture content. Fractal analysis indicated that regardless of the sand moisture content, termite tunnel geometry had a fractal dimension and termites generally tunneled more in higher moisture sand.