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.     

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.     

Buying time for colony mates: the anti-predatory function of soldiers in the eusocial aphid Ceratovacuna japonica (Homoptera, Hormaphidinae)

Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species’ natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator’s body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers’ colony mates time to reproduce or to escape from the predator.     

Soldier caste influences on candidate primer pheromone levels and juvenile hormone-dependent caste differentiation in workers of the termite Reticulitermes flavipes

Caste systems and the division of labor they make possible are common underlying features of all social insects. Multiple extrinsic factors have been shown to impact caste composition in social insect colonies. Primer pheromones are one type of extrinsic caste-regulatory factor; they are chemical signaling molecules produced by certain colony members to impact developmental physiology of recipient nestmates. However, only limited evidence exists regarding primer pheromones and their actions in eusocial termites. In previous research we identified two soldier-produced terpenes, γ-cadinene (CAD) and γ-cadinenal (ALD), as candidate primer pheromones of the lower termite Reticulitermes flavipes. In the present study we tested hypotheses related to CAD and ALD action in recipient individuals. We examined the influences of terminally developed soldier termites on (1) CAD and ALD levels and (2) caste differentiation in developmentally totipotent workers. Our findings show CAD and ALD (respectively) are caste stimulatory and inhibitory components of chemical blends present in soldier heads, ALD levels increase significantly (10.9×) in workers only in the presence of soldiers, and soldiers can reduce developmental-hormone response thresholds of workers, presumably via ALD action. These findings provide novel evidence supporting that CAD and ALD are authentic caste-regulatory primer pheromones in Reticulitermes.     

Community structure and antifungal activity of actinobacteria in a fungus-growing termite

1. Fungus-growing termites cultivate the fungal mutualist Termitomyces as their main food source; however, how fungus-growing termites protect Termitomyces from threats is still unclear. In this study, we investigated the actinobacterial communities in Odontotermes formosanus individuals and their fungal combs.
2. Moreover, the antifungal activities of the isolated actinobacteria were tested. 16 S rRNA gene sequencing results indicated that the actinobacteria in O. formosanus and its fungal combs belong to 5 classes, 17 orders, 40 families, and 84 genera.
3. The relative abundance of Coriobacteriia in the nymphs, young workers, old workers, and soldiers was higher than that in the queens and fungal combs, and the relative abundance of class Actinobacteria in the queens and the fungal combs was higher than that in the nymphs, young workers, old workers, and soldiers.
4. Based on antifungal bioassays, 3 strains of Amycolatopsis and 2 strains of Streptomyces isolated from old workers had strong inhibitory activity against Xylaria angulosa but weak inhibitory activity against Termitomyces sp.
5. These results indicated that the actinobacteria of O. formosanus may contribute to protecting termite fungal food via their asymmetric antifungal activities.

     

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.     

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.     

Cuticular Hydrocarbons of Reticulitermes (Isoptera: Rhinotermitidae) from Northern California Indicate Undescribed Species

Cuticular hydrocarbon mixtures of Reticulitermes samples from disparate locations in northern California were characterized and correlated with species determinations. Literature records indicate that there are two extant species of Reticulitermes in northern California: Reticulitermes hesperus Banks and R. tibialis Banks. We identified five distinct hydrocarbon phenotypes in Reticulitermes from northern California. Termites were diagnosed morphologically as R. tibialis for all five cuticular hydrocarbon phenotypes based on available keys to soldiers. Commonly accepted distributions of Reticulitermes in northern California indicate that our primary collection sites should only produce R. hesperus. On the basis of cuticular hydrocarbons alone we suggest that there are two or more undescribed taxa of Reticulitermes in northern California, or that described species of Reticulitermes occur in northern California, but have never been noticed before. Therefore, we conclude that the taxonomy of Reticulitermes in North America is in need of revision.     

Response variability of juvenile hormone and juvenile hormone analogs in workers of the Formosan subterranean termite (Coptotermes formosanus Shiraki)

Juvenile hormone (JH) or juvenile hormone analog (JHA) can induce soldier formation in termites. However, different studies have yielded inconsistent results on the effects of JHA on soldier production in Coptotermes formosanus Shiraki. Using filter paper as the testing substrate, the effects of JH III, pyriproxyfen and methoprene on the intact filter paper left, worker mortality and presoldier formation were tested on six colonies. Our results showed that pyriproxyfen and methoprene were more repellent than JH III. No significant difference in toxicity was observed among methoprene, pyriproxyfen and JH III. JH III and pyriproxyfen did not cause workers to differentiate into presoldiers, but methoprene can induce formation of presoldiers. Colony response variability to methoprene was observed. The confirmation of the effects of JH/JHA on C. formosanus establishes the foundation for molecular studies of soldier differentiation in this species.     

Predator biodiversity increases the survivorship of juvenile predators

When predator biodiversity strengthens herbivore suppression, the pattern generally is attributed to interspecific complementarity. However, the relaxation of intraspecific interference within diverse communities has received less attention as an underlying factor, and most experiments to date span much less than one predator generation. Here, working with a community of aphid predators, we compared the survivorship of juvenile predators embedded within diverse versus single-species communities of adult predators. We found that greater predator diversity improved juvenile survivorship for three of four predator taxa (the lady beetles Hippodamia convergens and Coccinella septempunctata, and the bug Nabis alternatus; but not the small bug Geocoris bullatus), whereas survivorship was relatively low when juveniles foraged among only conspecific adults. When aphid densities differed they were lowest for the diverse treatment, and so resource availability could not explain differences in juvenile survivorship. Instead, feeding trials indicated that cannibalism generally posed a greater risk to juveniles than did intraguild predation (with Geocoris again the exception). Our results suggest that the dilution of intraspecific interference may play an important, and perhaps underappreciated, role in shaping predator diversity effects. Furthermore, relatively strong cannibalism but weak intraguild predation has the potential to project diversity effects forward into subsequent generations.     

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

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

Socio-environmental and endocrine influences on developmental and caste-regulatory gene expression in the eusocial termite <Emphasis Type="Italic">Reticulitermes flavipes</Emphasis>

Background  

Strict regulation of caste differentiation, at the molecular level, is thought to be important to maintain social structure in insect societies. Previously, a number of extrinsic and intrinsic factors have been shown to influence caste composition in termite colonies. One important factor is the influence of nestmates; in particular, soldier termites are known to inhibit hormone-dependent worker-to-soldier differentiation. However, soldier influences on nestmates at the molecular level are virtually unknown. Here, to test the hypothesis that soldiers can influence nestmate gene expression, we investigated the impact of four treatments on whole-body gene expression in totipotent Reticulitermes flavipes workers: (i) juvenile hormone III (JHIII; a morphogenetic hormone), (ii) soldier head extracts (SHE), (iii) JHIII+SHE, and (iv) live soldiers.     

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.     

Endogenous synchronization of the chemical signature of Reticulitermes (Isoptera: Rhinotermitidae) worker termites

Termites of the genus Reticulitermes are characteristic of temperate regions. Their colonies comprise various castes, the most numerous being that of workers which can develop into soldiers or secondary reproductives (neotenics). Each caste has a mixture of hydrocarbons (HCs) on the cuticle forming a chemical signature. The primary aim of this study was to compare the changes in the chemical signature of a population of worker termites fed on paper with juvenile hormone to differentiate them into soldiers with a control population of termites fed only on paper or wood for one month. Gas chromatography was used to analyze the cuticular profiles of Reticulitermes flavipes termites to determine whether they changed, and, if so, when and how. The data collected over one month showed that the workers fed with JH did not differentiate into soldiers but that there were progressive changes in the hydrocarbon profile independent of the treatment. These results indicate that the differentiation of the chemical signature of the worker caste is a dynamic process, depending only on time and not on colony membership, confirming that, for these termites, this signature has a lesser role in colony membership than caste membership, unlike the chemical signatures of other social insects. The temporal process of this cuticular change is also associated with a change in the alkene/methyl-branched alkane ratio.     

The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation on Aedes triseriatus

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Intracolonial differences in gut bacterial community between worker and soldier castes of Coptotermes formosanus

Abstract The establishment of symbiotic relationships with intestinal microorganisms enables termites to thrive on recalcitrant substrates such as cellulose and wood. A termite colony is composed of several different castes which have distinct feeding habits. The soldiers, for example, cannot feed by themselves and depend on workers, who feed them with digested or semi‐digested foods. To investigate the influence of feeding habits on the bacterial symbionts, a comparative study of gut bacteria between worker and soldier castes of the termite Coptotermes formosanus was conducted. The bacterial communities of both castes were investigated using denaturing gradient gel electrophoresis (DGGE) and clonal analysis of 16S ribosomal DNA (rDNA). Both methods indicated Bacteroidetes was the common predominant group; the common dominant phylotype was affiliated with a reported uncultured Bacteroidetes phylotype (BCf1–03). There were significant differences in Bacteroidetes and Spirochaetes between two castes. Compared to the gut bacteria of workers, those of soldiers were lower in abundance and diversity of Bacteroidetes and slightly higher in Spirochaetes. Two phylotypes (W8, W11) affiliated to Bacteroidetes and two (W26, W29) affiliated to Spirochaetes were exclusively found in the DGGE profile of the worker caste. Bacteroidetes are assumed to be involved in fermentation of sugars and nitrogenous compounds as well as degradation of uric acid. Spirochaetes are supposed to aid in the functions of acetogenesis and N₂‐fixation. The different feeding habits between workers and soldiers of C. formosanus may explain the observed differences in the gut bacterial community.     

Panic escape polyethism in worker and soldier Coptotermes formosanus (Isoptera: Rhinotermitidae)

Termites were the first animal to form societies. Two hundred million years of evolution provide for a multitude of innate social behaviors that can be experimentally dissected. These fine‐tuned patterns of behavior are especially interesting when observing group decision making in the panic mode. In this study, we examined behavioral patterns of termites under panic conditions to gain insight into how an escape flow self‐organizes. One hundred worker and 10 soldier Coptotermes formosanus were released into agar plates. After a disturbance was created most workers followed each other and ran along the wall of dishes, thus forming a unidirectional escape flow, whereas soldiers showed a significantly higher frequency of moving to the center of the arena or on periphery of the escape flow as compared to workers. Agonistic behavior was usually observed as soldiers moved to center or periphery. This is the first report on the behavioral repertoire of termites when panicked, with details on the behavioral polymorphism of workers and soldiers during an escape.     

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 .     

Light alters activity but does not disturb tandem coordination of termite mating pairs

Group-living animals coordinate their movements via local interactions, which can be mediated by visual, tactile, and chemical communication channels. Termite mating pairs form tandems with one male imago following one female imago in a synchronised way to explore the environment and search for a nesting site. Imagoes are the only developmental stage with compound eyes in termites, but the role of vision during tandem runs remains unknown. Here, we investigate the movements during tandem runs of two termite species, Coptotermes formosanus, which swarms during the night, and Reticulitermes speratus, which swarms during the day. We performed the experiments with light and in complete darkness. We found that females and males of both species adjust their speed to each other to form a stable tandem and reunite efficiently upon separation, with or without light. However, the activity was dependent on light conditions in the diurnal R. speratus, in which termites were more active with light. On the other hand, the nocturnal C. formosanus was mostly insensitive to light environments, with termites being slightly more active in darkness. Our results suggest that termites can use light as an environmental cue to start forming mating pairs but not as means to locate mates or coordinate their movements.     

Termite salinity tolerance and potential for transoceanic dispersal through rafting

1. Oceanic rafting through driftwood has been hypothesized to be a mechanism underlying the transoceanic distribution of termites (Order: Blattodea). To test this hypothesis, we examined the salinity tolerance of 12 termite species from eight genera and three families, namely Archotermopsidae, Kalotermitidae, and Rhinotermitidae.
2. Our results revealed that the survival rates of Incisitermes inamurai (Oshima), Cryptotermes domesticus (Haviland), Prorhinotermes flavus (Bugnion and Popoff), P. simplex (Hagen), and Heterotermes sp. are not affected by treatment with 3.5% saline water, strongly supported that oceanic rafting may be a mechanism underlying the insects' transoceanic distribution.
3. By contrast, Hodotermopsis sjostedti Holmgren, Glyptotermes satsumensis (Matsumura), Coptotermes formosanus Shiraki, Co. gestroi (Wasmann), Reticulitermes virginicus (Banks), R. leptomandibularis Hsia and Fan, and R. kanmonensis Takematsu treated with saline water showed dehydration symptoms, and their mortality rates increased significantly within 12 days after treatment. These results indicate that these species are less likely to be dispersed through oceanic driftwood and that their transoceanic dispersal is rather more likely to occur through human transportation or land bridges.
4. Phylogenetic positions and habitats of salinity‐tolerant termites implied that the acquisition of salinity tolerance may relate to both phylogeny and coastal living.