Tetramorium Tsushimae Research Articles

A checklist of ants (Hymenoptera: Formicidae) in northern Shaanxi Province, China, with one new species of genus Proformica Ruzsky, 1902

• A new species Proformica muusensis sp. nov. , is described. • Seven species from Shaanxi Province are reported for the first time. • A preliminary checklist of ants of the northern Shaanxi is provided. A preliminary checklist of the ants of northern Shaanxi is presented based on an evaluation from June 2018 to September 2020. Seven species are reported from Shaanxi for the first time: Formica approximans Wheeler, 1933; Formica clara Forel, 1886; Messor aralocaspius (Ruzsky, 1902); Plagiolepis pygmaea (Latreille, 1798); Tapinoma rectinotum Wheeler, 1927; Tetramorium chefketi Forel, 1911; Tetramorium tsushimae Emery, 1925 and Temnothorax ruginosus Zhou, Huang, Yu & Liu, 2010. A new species of genus Proformica Ruzsky, 1902, Proformica muusensis sp. nov. , is described based on the morphology and molecular method. In total, three subfamilies with 34 valid ant species in 15 genera are reported in our checklist.

The complete mitochondrial genome of Tetramorium tsushimae (Emery, 1925) (Hymenoptera: Formicidae)

Tetramorium tsushimae (Emery, 1925) is an omnivorous ant species native to East Asia and has been introduced to North America. The mitochondrial genome of T. tsushimae is 19,207 bp in length with an A + T content of 81.3% and includes 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNAs, and a control region. This sequence data would play an important role in the investigation of mitochondrial evolution of the subfamily Myrmicinae.

Effect of social structure and introduction history on genetic diversity and differentiation

Invasive species are a global threat to biodiversity, and understanding their history and biology is a major goal of invasion biology. Population-genetic approaches allow insights into these features, as population structure is shaped by factors such as invasion history (number, origin and age of introductions) and life-history traits (e.g., mating system, dispersal capability). We compared the relative importance of these factors by investigating two closely related ants, Tetramorium immigrans and Tetramorium tsushimae, that differ in their social structure and invasion history in North America. We used mitochondrial DNA sequences and microsatellite alleles to estimate the source and number of introduction events of the two species, and compared genetic structure among native and introduced populations. Genetic diversity of both species was strongly reduced in introduced populations, which also differed genetically from native populations. Genetic differentiation between ranges and the reduction in microsatellite diversity were more severe in the more recently introduced and supercolonial T.tsushimae. However, the loss of mitochondrial haplotype diversity was more pronounced in T.immigrans, which has single-queen colonies and was introduced earlier. Tetramorium immigrans was introduced at least twice from Western Europe to North America and once independently to South America. Its monogyny might have limited genetic diversity per introduction, but new mutations and successive introductions over a long time may have added to the gene pool in the introduced range. Polygyny in T.tsushimae probably facilitated the simultaneous introduction of several queens from a Japanese population to St. Louis, USA. In addition to identifying introduction pathways, our results reveal how social structure can influence the population-genetic consequences of founder events.

Forensic implication of cadaveric behaviors of the Japanese pavement ant (Tetramorium tsushimae Emery) attending to rabbit cadavers

AbstractIt is noticed by some researchers that ants may cause some forensic confusion in understanding death scenes. In the aspect of relationship between the ant‐animal decomposition, we observed the behavior of ants congregating on dead animals. Amongst various species of ants visiting dead rabbits, Tetramorium tsushimae Emery was noticeable in producing scratched scars, mounds, and nests around dead rabbits and covering them with soils. The behaviors are likely to interfere or to disturb the usual process of decomposition succession lead by maggots. We discussed that a series of cadaveric behaviors of T. tsushimae may be used as a potential forensic hint not to misunderstand death scenes disturbed by the species.

Structure of ant assemblages on street trees in urban Busan, Korea

AbstractStreet trees planted in urban areas are one of the smallest urban green habitats; however, their role as a valuable refuge for local biota is poorly understood. The aim of this study was to investigate urban street trees as habitat for ants. We found ants on 195 (92%) of 211 street trees studied. Seventeen ant species were collected from five tree species. The two most common ant species were Tetramorium tsushimae (on 112 trees) and Lasius japonicus (on 93 trees). The number of ant species found per tree ranged from 0 to 5, with a mean of 1.55 ± 0.92. The species composition differed significantly among tree species. Nine ant species (Camponotus vitiosus, Lasius alienus, L. japonicus, Nylanderia flavipes, Crematogaster matsumurai, Crematogaster vagula, Monomorium intrudens, T. tsushimae, and Brachyponera chinensis) nested on the trees, mostly in the root zone. Nests were found on 150 trees but were relatively rare on trees with diameter at breast height of less than 40 cm.

Seed dispersal by the omnivorous ant Tetramorium tsushimae Emery (Formicidae) in three common weed species

The Japanese pavement ant Tetramorium tsushimae Emery (Formicidae) is a species of seed-collecting ant found in Japan. However, its role in seed dispersal has not yet been satisfactorily documented. We investigated the seed-carrying behaviour of T. tsushimae both in the laboratory and in the field. In the laboratory, seeds of three common weeds [evening primrose Oenothera biennis (Onagraceae), purslane Portulaca oleracea (Portulacaceae), and dropseed Sporobolus fertilis (Poaceae)] were examined. More than 65% of each kind of seed was carried by the ants, but some were later discarded outside the nest. Among the three, S. fertilis seeds were collected most frequently. The germination rate of the seeds was higher than 80% for both discarded and stored O. biennis and S. fertilis seeds but lower than half for discarded P. oleracea seeds. In the field, the relationship between the ants and the growing locations of O. biennis or P. oleracea was investigated. The distribution of O. biennis plants considerably overlapped with the distribution of T. tsushimae nest holes at all survey sites. The distribution of P. oleracea also overlapped with that of ant nest holes at some sites. In areas where O. biennis and P. oleracea were absent, a high proportion (> 65%) of artificially placed seeds were carried by T. tsushimae. A few months later, O. biennis seedlings were observed near many ant nest holes. The mean distance between the seedlings and seed-set point was 7.2 m. Although P. oleracea seeds were observed near nest holes, their seedlings were not detected. The present results suggest that O. biennis plants benefit from seed dispersal by T. tsushimae and that the distribution of P. oleracea plants might also be influenced by ant foraging behaviour.

Winter Activity of Ants in an Urban Area of Western Japan

During winter, foraging activity of ants is considered low in temperate regions. Winter activity of ground-dwelling ants was investigated using bait traps and quadrat sampling in an urban area of Fukuoka City, western Japan. Six study sites were grouped into two categories: 4 open land types and 2 forest types. A total of 18 ant species were recorded between the end of January and beginning of March. The foraging activity of ants was generally low, except during relatively warm periods when the surface ground temperature was above 6℃–7℃ or soil temperature was above 4℃–5℃. Tetramorium tsushimae, Messor aciculatus, and Pheidole noda were the most abundant in the open land type, whereas Nylanderia flavipes, P. noda, and Crematogaster osakensis were the most abundant in the forest type. Bait preference varied among the different species, e.g., P. noda preferred tuna over honey, whereas N. flavipes similarly responded to tuna and honey. This is the first detailed study on the relationship between temperature and ant activity in Japanese mainland fauna.

Identification of methyl 6-methylsalicylate as the trail pheromone of the Japanese pavement ant Tetramorium tsushimae (Hymenoptera: Formicidae)

The Japanese pavement ant Tetramorium tsushimae Emery (Hymenoptera: Formicidae) has a mass recruitment system for foraging. We successfully separated the trail pheromone from the ant worker extract by preparative gas chromatography, and estimated it as methyl 6-methylsalicylate based on the Kovats retention indices and mass spectra, which coincided with those of the synthetic compound. We also confirmed that the synthetic methyl 6-methylsalicylate elicited a trail-following response in the workers even at approximately 0.3 pg/cm of the trail line. The strength for this response was similar to the estimated level of trail pheromone in the abdominal extracts of workers. It seems likely that the glandular source was the poison gland, because poison gland extract evoked trail-following responses in significantly more workers than other gland extracts. We therefore identified the trail pheromone of this ant species as methyl 6-methylsalicylate and tentatively identified its source as the poison gland.

Effects of Attending Ant Species on the Fate of Colonies of an Aphid, Macrosiphoniella yomogicola (Matsumura) (Homoptera: Aphididae), in an Ant-Aphid Symbiosis

An aphid, Macrosiphoniella yomogicola, establishes an obligate symbiosis with ants and cannot survive without attending ants. Several species of ant attend this aphid, but differences in the effects of attending ant species on the fate of aphid colonies are unknown. Here, we report that parasitism rates by parasitic wasps and the survival of aphid colonies differ depending on the species of attending ants in this symbiotic system in autumn 2017. the proportions of mummies (parasitized aphid individuals) were significantly higher in colonies attended by ants (tetramorium tsushimae and Pheidole fervida) other than lasius japonicus, which is the most abundant attender. Only the aphid colonies attended by l. japonicus survived to the end of the observational period. Our results indicate that the species of attending ant has a crucial effect on the fate of symbiotic aphid colonies.

Combined use of two defensive traits in pupae of Scymnus posticalis ladybirds

AbstractCoccinellid pupae have various defensive traits, such as keeping their final‐instar larval exuviae and secreting droplets containing defensive chemicals at the tips of glandular hairs. Although each of these traits has been described separately in different species, it is unclear how each defensive trait functions when more than one trait coexists. We found that pupae of the ladybird Scymnus posticalis have two different types of traits; they were partially covered with their own final‐instar larval exuviae, with thick wax structures, and had many glandular hairs secreting transparent droplets on the exposed parts of the body without waxy exuviae (head and medial parts of thoracic and abdominal dorsum). In this study, the defensive effects of these two traits were evaluated against two ant species, Tetramorium tsushimae and Lasius japonicus, which are potential predators. When encountering a pupa, neither ant species were able to make frequent physical contact with the exposed parts of the pupa because of the presence of the waxy exuviae. When touching the exposed body part that was covered with droplets, both ant species immediately stepped backward and then swept their antennae. The droplets suppressed ant feeding when mixed with sucrose solution, suggesting that the droplets contain repellent chemicals. These results indicate that the two traits of S. posticalis pupae (the larval waxy exuviae and the droplets) effectively play defensive roles against ants, functioning as a physical obstruction and a chemical repellent, respectively.

Tetramorium tsushimae Ants Use Methyl Branched Hydrocarbons of Aphids for Partner Recognition.

In mutualisms, partner discrimination is often the most important challenge for interacting organisms. The interaction between ants and aphids is a model system for studying mutualisms; ants are provided with honeydew by aphids and, in turn, the ants offer beneficial services to the aphids. To establish and maintain this system, ants must discriminate mutualistic aphid species correctly. Although recent studies have shown that ants recognize aphids as mutualistic partners based on their cuticular hydrocarbons (CHCs), it was unclear which CHCs are involved in recognition. Here, we tested whether the n-alkane or methylalkane fraction, or both, of aphid CHCs were utilized as partner recognition cues by measuring ant aggressiveness toward these fractions. When workers of Tetramorium tsushimae ants were presented with dummies coated with n-alkanes of their mutualistic aphid Aphis craccivora, ants displayed higher levels of aggression than to dummies treated with total CHCs or methyl alkanes of A. craccivora; responses to dummies treated with n-alkanes of A. craccivora were similar to those to control dummies or dummies treated with the CHCs of the non-mutualistic aphid Acyrthosiphon pisum. By contrast, ants exhibited lower aggression to dummies treated with either total CHCs or the methylalkane fraction of the mutualistic aphid than to control dummies or dummies treated with CHCs of the non-mutualistic aphid. These results suggest that T. tsushimae ants use methylalkanes of the mutualistic aphid's CHCs to recognize partners, and that these ants do not recognize aphids as partners on the basis of n-alkanes.

Social transmission of information about a mutualist via trophallaxis in ant colonies.

Partner discrimination is crucial in mutualistic interactions between organisms to counteract cheating by the partner. Trophobiosis between ants and aphids is a model system of such mutualistic interaction. To establish and maintain the mutualistic association, ants need to correctly discriminate mutualistic aphids. However, the mechanism by which ants recognize aphids as their partners is poorly understood, despite its ecological and evolutionary importance. Here, we show for the first time the evidence that interaction with nest-mates that have tended aphids (Aphis craccivora) allows ants (Tetramorium tsushimae) to learn to recognize the aphid species as their partner. When ants had previously tended aphids, they moderated their aggressiveness towards aphids. More importantly, ants that had interacted with aphid-experienced nest-mates also reduced their aggressiveness towards aphids, even though they had never directly experienced them, indicating that aphid information was transmitted from aphid-experienced ants to inexperienced ants. Furthermore, inhibition of mouth-to-mouth contact (trophallaxis) from aphid-experienced ants to inexperienced ants by providing the inexperienced ants with artificial honeydew solution caused the inexperienced ants to become aggressive towards aphids. These results, with further supporting data, strongly suggest that ants transfer information on their mutualists during trophallactic interactions.

Paternal care behaviour of the giant water bug Kirkaldyia deyrolli (Heteroptera: Belostomatidae) against ants

1. Although potentially vulnerable to predators, the offspring of subsocial insects are effectively protected by their parent(s). The female giant water bug Kirkaldyia deyrolli lays its egg masses on the vegetation above the water surface in aquatic environments and the males supply the eggs with water and guard them against cannibalistic females until hatchling dispersal. Field observations showed that egg masses are attacked by ants if the attending males are not present.2. Laboratory experiments were conducted to evaluate the effects of paternal care by K. deyrolli against the ant Tetramorium tsushimae by means of four treatments: attending male with ant approach (WM‐WA); no attending male with ant approach (NoM‐WA); attending male without ant approach (WM‐NoA); and no attending male without ant approach (NoM‐NoA).3. The rate of offspring survival was lower in the NoM‐WA group (45.3%) than in any other group, which showed similar offspring survival (WM‐WA = 80.4%, WM‐NoA = 75.1%, NoM‐NoA = 80.3%). Moreover, there were a total of 44 interactions between the attending male and ants in WM‐WA, and of these, a chemical compound was released by the attending male four times; this probably deterred ants from attacking because the ants went back to their colony.4. In conclusion, the attending male can protect its eggs from ant predators and its care has an important role. To the best of the authors' knowledge, this is the first report of Lethocerinae males protecting their egg masses from ants by means of physical and chemical defence.

Efficacy of Chemical Mimicry by Aphid Predators Depends on Aphid-Learning by Ants.

Chemical mimicry is an effective strategy when signal receivers recognize and discriminate models by relying on chemical cues. Some aphid enemies mimic the cuticular chemicals of aphids through various means thus avoiding detection and attack by aphid-tending ants. However, because ants have been reported to learn the chemical signatures of aphids in order to distinguish the aphids, the efficacy of chemical mimicry is predicted to depend on the experience of the ants that had tended aphids. The present study tested this hypothesis using two predator species: larvae of the green lacewing Mallada desjardinsi, and larvae of the ladybeetle Scymnus posticalis. Lacewing larvae carry the carcasses of aphids on which they have preyed upon their backs, and these function via chemical camouflage to reduce the aggressiveness of aphid-tending ants toward the larvae. Ladybeetle larvae reportedly produce a covering of wax structures, and their chemicals appear to attenuate ant aggression. We examined whether the behavior of the ant Tetramorium tsushimae toward these predators changed depending on their aphid-tending experience. Ants moderated their aggressiveness toward both predators when they had previously tended aphids, indicating that chemical mimicry by both aphid predators is dependent on previous experience of the ants in tending aphids. Chemical mimicry by the predators of ant-tended aphids is therefore considered to exploit learning-dependent aphid recognition systems of ants.

Ants Learn Aphid Species as Mutualistic Partners: Is the Learning Behavior Species-Specific?

In ant-aphid associations, many aphid species provide ants with honeydew and are tended by ants, whereas others are never tended and are frequently preyed upon by ants. In these relationships, ants must have the ability to discriminate among aphid species, with mutualistic aphids being accepted as partners rather than prey. Although ants reportedly use cuticular hydrocarbons (CHCs) of aphids to differentiate between mutualistic and non-mutualistic species, it is unclear whether the ability to recognize mutualistic aphid species as partners is innate or involves learning. Therefore, we tested whether aphid recognition by ants depends on learning, and whether the learning behavior is species-specific. When workers of the ant Tetramorium tsushimae had previously tended the cowpea aphid, Aphis craccivora, they were less aggressive toward this species. In addition, ants also reduced their aggressiveness toward another mutualistic aphid species, Aphis fabae, after tending A. craccivora, whereas ants remained aggressive toward the non-mutualistic aphid, Acyrthosiphon pisum, regardless of whether or not they had previous experience in tending A. craccivora. When ants were offered glass dummies treated with CHCs of these aphid species, ants that had tended A. craccivora displayed reduced aggression toward CHCs of A. craccivora and A. fabae. Chemical analyses showed the similarity of the CHC profiles between A. craccivora and A. fabae but not with A. pisum. These results suggest that aphid recognition of ants involves learning, and that the learning behavior may not be species-specific because of the similarity of CHCs between different aphid species with which they form mutualisms.

Seed dispersal of the hemiparasitic plant Thesium chinense by Tetramorium tsushimae and Pristomyrmex punctatus

AbstractHeterotrophic plants normally produce a vast number of dust‐like seeds containing minimal energy reserves, which are usually wind dispersed. However, some heterotrophic species have evolved adaptive strategies to use zoochorous seed dispersal. Seed dispersal by ants, known as myrmecochory, is one of the most widespread animal dispersal systems and has been reported in a diverse range of plant taxa. However, the combination of myrmecochory and heterotrophy seems to be very rare. Here I report the discovery of myrmecochory in the hemiparasitic plant Thesium chinense by Tetramorium tsushimae and Pristomyrmex punctatus. Myrmecochory would be an advantageous dispersal system for T. chinense because its fruits are quickly transferred to the ants' nests, which provide a refuge from the seed predator Canthophorus niveimarginatus. Myrmecochory is also potentially beneficial for T. chinense, as the nests of these ants are frequently located close to poaceous plants, which are the preferred hosts.

Adaptive Advantage of Myrmecochory in the Ant-Dispersed Herb Lamium amplexicaule (Lamiaceae): Predation Avoidance through the Deterrence of Post-Dispersal Seed Predators.

Seed dispersal by ants (myrmecochory) is found worldwide, but the benefits that plants obtain from this mutualism remain uncertain. In the present study, we conducted laboratory experiments to demonstrate seed predator avoidance as a benefit of myrmecochory using the annual ant-dispersed herb Lamium amplexicaule, the disperser ant Tetramorium tsushimae, and the seed predatory burrower bug Adomerus rotundus. We compared the predation intensity of Lamium amplexicaule seeds by Adomerus rotundus under the presence or absence of Tetramorium tsushimae. Both the number of seeds sucked by Adomerus rotundus adults and the feeding duration of sucked seeds by nymphs were significantly reduced in the presence of ants. This effect was most likely due to the behavioral alteration of Adomerus rotundus in response to the ant presence, because ants seldom predated Adomerus rotundus during the experiment. Our results demonstrated that the presence of ants decreases post-dispersal seed predation, even when the ants do not bury the seeds. The present study thus suggests that the non-consumptive effects of ants on seed predators benefit myrmecochorous plants.

Differential dispersal of Chamaesyce maculata seeds by two ant species in Japan

Seed dispersal by ants (myrmecochory) is a widely distributed plant–animal interaction in many ecosystems, and it has been regarded as a generalized (multiple species) interaction in which specialization on specific ant partners is uncommon. In this paper, we demonstrate species-specific seed dispersal of spotted spurge (Chamaesyce maculata) by ants in Japan. C. maculata produces seeds from summer to autumn in Japan. The seeds produced in autumn are carried by two ant species, Tetramorium tsushimae and Pheidole noda. We performed laboratory experiments to investigate the fate of C. maculata seeds in the nests of T. tsushimae and P. noda. P. noda consumed the seeds in the nest and rarely carried seeds out of the nest, while T. tsushimae consumed only the seed coat, and subsequently carried the seeds out of the nest. Removal of the seed coat by T. tsushimae may increase seed survival by reducing their susceptibility to infection by fungi. We also observed ant responses to filter paper soaked with an aqueous extract of the seed coat. P. noda did not react to the filter paper, but T. tsushimae carried the filter paper into their nest. Analysis by high-pressure liquid chromatography revealed that the aqueous extract contained at least four sugars and one unknown substance. Myrmecochory has been regarded as a generalized interaction with specialization for specific ant partners uncommon. However, our study suggests there is a species-specific interaction in seed dispersal by ants in autumn-flowering individuals of C. maculata in Japan.

Seed predator deterrence by seed‐carrying ants in a dyszoochorous plant, Chamaesyce maculata L. Small (Euphorbiaceae)

Seeds are often carried by omnivorous ants even if they do not carry elaiosomes. Although many seeds carried by ants are consumed, both seeds abandoned during the seed carrying and leftover seeds are consequently dispersed (dyszoochory). These non-myrmecochorous seeds do not necessarily attract ants quickly. Therefore, these seeds often seem to be exposed to the danger of consumption by pre-dispersal seed predators. We propose the hypotheses, “seed predator deterrence hypothesis” that plants may benefit from seed-carrying ants if they deter seed predators from visiting plants, and seed-carrying ants may play additional roles in plant reproductive success, besides dyszoochory by ants. To test the hypotheses, we investigated the abundance of seed-carrying ants of the species Tetramorium tsushimae Linnaeus and Pheidole noda Smith F., and of the seed predatory stinkbug, Nysius plebeius Distat, on the spotted sandmat, Chamaesyce maculata L. Small, of which the seeds have no elaiosomes but are consumed by both ants and bugs. In the field, ants and stinkbugs seldom encountered each other on the plant. The number of stinkbugs beneath the plants with ants was smaller than that beneath the plants without ants. In laboratory experiments, the number of stinkbugs on the shoot was smaller when ants were present than when they were absent. These results might support the seed predator deterrence hypothesis: the probability of seed predation by stinkbugs seems to be reduced by the ant visits on plants and/or the existence of ants beneath the plants. This study highlights a new ant–plant interaction in seed dispersal by ants.

Extrafloral nectaries indirectly protect small aphid colonies via ant-mediated interactions

When ant-tended aphids parasitize plants with extrafloral nectaries (EFNs), ant-mediated indirect interactions occur between the plants and aphids. In particular, when an aphid colony is small, the honeydew production of the colony is insufficient to attract ants, although EFNs can attract many ants. Under this condition, we asked whether a small aphid colony would gain indirect benefits from EFNs because ants would be attracted by the EFNs instead of the aphids, or whether the aphid colony would suffer strong predatory pressure from ants and/or other predators. To clarify the aphid-plant interactions, the protective services provided by two ant species, Lasius japonicus and Tetramorium tsushimae, for the survival of a small colony of Aphis craccivora were examined on the host plant, Vicia faba, with and without EFNs. More workers of both ant species were recruited to the plants with EFNs than to those without EFNs, and the larvae of a predatory ladybird beetle, Coccinella septempunctata, stayed for a shorter time and preyed on a smaller number of aphids on the plants with EFNs than on those without EFNs. In addition, no negative effects of EFNs, such as predation of the aphids by the ants, were found. Consequently, it is suggested that a small aphid colony gains indirect benefits from the EFNs of its host plant.