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.     

A novel hypothesis for the origin of the sexual division of labor in termites: which sex should be soldiers?

Sexual specialization and skewed sex ratios of the altruistic castes, especially soldiers, are common in many termite taxa. However, no theoretical or empirical studies have explained the origin of the sexual division of labor in termites. In most termite species, female alates are larger than male alates, and mature queens are much larger than kings, with females under consistent selection for high fertility. Therefore, females usually have the potential to be larger than males. Here, I present a novel preadaptation hypothesis that potential sexual differences in the suitability for the caste give rise to the sexual division of labor, and I provide the first evidence in support of this hypothesis in termites. Defense in Reticulitermes is typically performed by soldiers via mandibular and phragmotic defense in which soldiers with pluglike heads block openings, thus preventing enemies from invading the nest. Phragmotic defense requires that soldiers have heads wide enough to plug nest openings. Therefore, a size threshold for workers that develop into soldiers is a likely adaptation for effective defense. I show that sexual size dimorphism (SSD) and a size threshold for soldiers promote skewed sex ratios. A female-biased soldier sex ratio was observed in species with SSD, whereas there was no bias in soldier sex ratio in species without SSD. Thus, SSD and soldier sex ratio data from several Reticulitermes species support the preadaptation hypothesis.     

X‐ray computed tomography reveals that intraspecific competition promotes soldier differentiation in a one‐piece nesting termite

Investment in soldier production in eusocial lineages involves a trade‐off between maintenance costs and defense benefits. Termites are eusocial insects that live in colonies organized into three castes: primary reproductives, soldiers, and workers or pseudergates. Neotermes chilensis (Blanchard) (Isoptera: Kalotermitidae) is a one‐piece nesting termite that nests and forages in a single piece of wood. Two scenarios may be of importance in a defense context of one‐piece nesting termites: during swarms, when colonies may be invaded by winged termites (alates) in search of a place to found a new colony, and when colonies of conspecifics are present within the same substrate. It was hypothesized that the ratio of soldiers to non‐soldiers would be higher at the onset of the swarming period and in substrates bearing more than one termite colony. A method based on X‐ray computed tomography (CT) was developed to study gallery connectivity in colonies of N. chilensis and caste composition within colonies. Computed tomography allowed the digital reconstruction of the galleries within the substrate, even when they belonged to different colonies, and was effective in distinguishing termites from substrate, and soldiers from reproductives and pseudergates. Using CT, the ratio of soldiers to non‐soldiers was shown to be highest in colonies within multicolonial scapes (i.e., neighboring colonies were present in the same substrate) during the swarming season, thus supporting our initial hypotheses. These results constitute a unique example of induced defenses arising from intraspecific interactions in termites.     

Worker aggression of ant Lasius japonicus enhanced by termite soldier–specific secretion as an alarm pheromone of Reticulitermes speratus

The subterranean termite Reticulitermes speratus usually nests in rotten wood trunks, which may also be occupied by the Japanese garden ant Lasius japonicus. Few battles were observed between them under ordinary circumstances because they inhabit separate nesting sites. However, once the termite nesting sites were artificially broken, the ant workers invaded and hunted the termites, although the termite soldiers fought against the ants. This study aims to confirm intra‐ and inter‐specific chemical interactions between the termite and ant. Solid phase microextraction–gas chromatograph (SPME‐GC) analyses revealed that R. speratus soldiers secreted caste‐specific sesquiterpene hydrocarbon when they were irritated. Both the hexane extract of the soldiers and its hydrocarbon fraction, as well as the crushed soldier bodies, attracted the soldiers but dispersed the workers when presented on the trails. We also confirmed that the soldier chemicals enhanced aggressiveness of L. japonicus, which rushed around the odor sources and hunted any termites that were present. These findings suggest that: (i) the soldier–specific secretion might serve as an alarm pheromone in termite chemical communication, in which components recruit soldiers and also warn the other colony members away; and (ii) termite communication is eavesdropped on by L. japonicus workers to locate and hunt the termites.     

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.     

Fire ant predation on native and introduced subterranean termites in the laboratory: effect of high soldier number in Coptotermes formosanus

Abstract.

• 1 Native Reticulitermes spp. Holmgren and the introduced Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) were exposed to predation in the laboratory by Solenopsis invicta Buren (Hymenoptera: Formicidae), a known predator of Reticulitermes.
• 2 In one experiment, both taxa contained the 2.4% soldiers commonly found in Reticulitermes. In a second experiment, Reticulitermes contained 2.4% and C.formosanus a more normal 18.3% soldiers.
• 3 When soldier proportions were equal, C.formosanus soldiers suffered less of a decrease in survivorship due to predation compared with Reticulitermes soldiers. Little difference was found between taxa in the effect of predation on termite workers or in the effect of termites on predator survivorship.
• 4 When soldier proportions were unequal, both C.formosanus castes suffered less from predation than those of Reticulitermes. Again, little difference was found in the effect of termites on ants.
• 5 C.formosanus showed less movement into new containers when soldier number was abnormally low, compared with both taxa with normal caste proportions.

     

It is not only group size: Soldiers also modulate the tolerance to insecticide in termites (Blattodea: Isoptera)

The survivorship of social insects is known to increase with group size, even in situations of stress, such as starvation and exposure to insecticides. However, in termites, studies have been undertaken only with workers, disregarding the possible effect of soldiers. The role of soldiers in the termite colonies goes beyond defense, mainly in Nasutitermes species. It is already known that soldiers initiate the foraging as well as improve the decision-making of food resources. Here, we evaluated the effect of group size and the presence of soldiers on exposure to sublethal doses of the insecticide imidacloprid in Nasutitermes corniger (Termitidae: Nasutitermitinae). To do so, toxicity bioassays were undertaken initially to determine the dose of the insecticide required to kill 50% of the N. corniger population (LD₅₀) to be used in the main experiments. Survival bioassays were then carried out with termite groups, with and without soldiers, in different sizes (6, 10, 14, 22, 26, 30 and 60), exposed and nonexposed to insecticide. In general, the mean time to death of termites increases linearly with group size. However, the mean time to death in groups with soldiers was significantly longer only in groups exposed to the insecticide. Our results indicate that soldiers can help to increase the tolerance of nasute termite groups to insecticides, in addition to the group size, as already shown in the previous study. The size of the group and social context could, therefore, modulate behavioral and/or physiological responses that enhance the ability to survive under stressful situations.     

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.     

Soldier-specific modification of the mandibular motor neurons in termites

Social insects exhibit a variety of caste-specific behavioral tendencies that constitute the basis of division of labor within the colony. In termites, the soldier caste display distinctive defense behaviors, such as aggressively attacking enemies with well-developed mandibles, while the other castes retreat into the colony without exhibiting any aggressive response. It is thus likely that some form of soldier-specific neuronal modification exists in termites. In this study, the authors compared the brain (cerebral ganglion) and the suboesophageal ganglion (SOG) of soldiers and pseudergates (workers) in the damp-wood termite, Hodotermopsis sjostedti. The size of the SOG was significantly larger in soldiers than in pseudergates, but no difference in brain size was apparent between castes. Furthermore, mandibular nerves were thicker in soldiers than in pseudergates. Retrograde staining revealed that the somata sizes of the mandibular motor neurons (MdMNs) in soldiers were more than twice as large as those of pseudergates. The enlargement of MdMNs was also observed in individuals treated with a juvenile hormone analogue (JHA), indicating that MdMNs become enlarged in response to juvenile hormone (JH) action during soldier differentiation. This enlargement is likely to have two functions: a behavioral function in which soldier termites will be able to defend more effectively through relatively faster and stronger mandibular movements, and a developmental function that associates with the development of soldier-specific mandibular muscle morphogenesis in termite head. The soldier-specific enlargement of mandibular motor neurons was observed in all examined species in five termite families that have different mechanisms of defense, suggesting that such neuronal modification was already present in the common ancestor of termites and is significant for soldier function.     

Skewed soldier sex ratio in termites: testing the size-threshold hypothesis

Social insect colonies contain multiple phenotypes, i.e. castes, and this caste polyphenism is often linked to sexual dimorphism. Unlike social hymenopterans, both termite sexes are diploid and contribute to helper-type tasks within the colony. Nonetheless, a biased sex ratio is frequently observed in termites, especially in soldiers. To explain this bias in soldier sex ratio, Matsuura (Evol. Ecol. 20: 565–574, 2006) postulated the existence of a size threshold for workers molting into soldiers. Under the influence of sexual size dimorphism (SSD), such a threshold was considered to indirectly favor one sex. We conducted a literature survey of sex ratio among termite soldiers and tested this size-threshold hypothesis using data for 67 termite species from a variety of termite lineages. We demonstrated the existence of a size threshold for individuals molting into soldiers, resulting in the acquisition of soldiers of only one sex in species exhibiting strong SSD. In species exhibiting weak SSD, the size threshold skews the sex ratio of soldiers, but does not necessarily cause the loss of one sex. Finally, we observed a prevalence of single-sex soldiers in the Termitidae, regardless of SSD, suggesting that the ancestral developmental mechanisms that constrain soldier differentiation from one sex are maintained in certain extant species.     

A trade‐off between antipredatory behavior and pairing competition produced by male‑male tandem running in three Reticulitermes species

Due to the omnipresent risk of predation, termites have evolved many antipredatory behaviors. The two related species Reticulitermes speratus and R. chinensis have been demonstrated to use homosexual tandem running to decrease individual predation risk after shedding their wings. In this study, we tested risk of predation in the termite R. flaviceps, which is distantly related to the above two species. We determined that homosexual tandem running also led to low individual predation risk in dealates of R. flaviceps. Moreover, by combining a predation model with a competition model, we observed a typical trade‐off phenomenon between antipredatory behavior and pairing competition produced by male?male tandem running in the above three Reticulitermes species. Our results indicated that male?male tandem running could effectively protect disadvantaged individuals from being caught, but disadvantaged individuals would be easily eliminated in pairing competition after male?male tandem running, suggesting that male?male tandem running can promote population evolution in termites by repeatedly removing the relatively inferior male individuals.     

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.     

Hunting strategy of a generalist ant species proposed as a biological control agent against termites

We studied the hunting behaviour of Myrmicaria opaciventris (Hymenoptera: Formicidae) in order to evaluate if it can be used as a biological control agent against the termites that damage sugarcane plantations. Hunting workers foraged in groups and recruited nestmates at short-range when they encountered large termite soldiers or groups of small termite workers. Differences in prey capture concerned the: (1) means of detection (from a distance or by contact); (2) termite body part seized (small termites seized by the body; large termites by an appendage); (3) percentages of prey abandoned; and (4) use of venom. The sting of the workers is spatulated implying a topical application of the venom on the prey. Large termites were stretched by several workers whose adherence to the substrate is facilitated by well-developed arolia and claws on the legs while others spread venom on the body and carved it up. An adaptation to termite capture was noted with a distribution of tasks between the workers which subdued prey, and those which transported it. In the former case, the workers easily eliminated termite soldiers, successively attacked several termite workers and even captured new individuals while holding the first ones captured between their mandibles before retrieving them all at once. The remaining individuals were retrieved by the transporting workers. Given this particularly effective predatory strategy, we concluded that, under certain conditions, M. opaciventris can be used as a biological control agent against termites.     

八种白蚁的兵蚁和工蚁消化道形态比较研究(等翅目)

为探讨白蚁消化道形态品级差异及其系统学意义,对4个科8种白蚁兵蚁和工蚁的消化道进行比较形态学研究.结果表明:低等白蚁的兵蚁和(拟)工蚁形态较为相似,高等白蚁的兵蚁与工蚁局部特征存在明显差异.由低等到高等兵蚁和工蚁消化道各部分差异呈增多趋势.前、中、后肠占消化道的百分比在山林原白蚁Hodotermopsis sjoest...     

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.     

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

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

The aardwolf (Proteles cristatm Sparrman) 1783 as predator of termites*

(1) Food selection of aardwolves was studied by a comparison of faecal contents with available termite populations. Observations are reported on the foraging behaviour, and on aspects of termite biology which expose various species to predation. (2) The aardwolf diet shows a very high selectivity for one species of termite, Trinervitermes bettonianus in the Serengeti and ecologically similar species elsewhere. (3) Both morphology and foraging behaviour are very well adapted to feeding on Trinervitermes bettonianus or similarly behaving termites. The aardwolf does not dig for food; hearing is probably an important sense used for locating prey. (4) Various aspects of the termites' protection against aardwolf predation are discussed. (5) The aardwolf diet shows an increase in variety during the rains; the cause of this is discussed. (6) Some brief notes are made about territorial behaviour, scent marking and the use of middens. (7) As a management recommendation regular grassland burning is suggested for areas where the presence of aardwolves is considered desirable.     

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.