Ant Attendance Research Articles

Myrmecophilous butterflies utilise ant–treehopper associations as visual cues for oviposition

1. Selection of a safe oviposition site is important for herbivorous insects whose immature stages have limited mobility. Female herbivores rely on environmental cues for this choice, and presence of natural enemies or mutualistic partners may be important in this process.2. Some butterflies have mutualistic interactions with ants (myrmecophily), in which caterpillars offer a nutritional liquid and gain protection against natural enemies. Participants in butterfly–ant mutualisms may utilise signals to initiate interactions, but the use of visual cues by ovipositing myrmecophilous butterflies remains uncertain.3. Larvae of facultatively myrmecophilous Parrhasius polibetes (Lycaenidae) feed on Schefflera vinosa, and females prefer to oviposit near aggregations of the ant‐tended treehopper Guayaquila xiphias, where caterpillars survive better due to increased ant attendance. Given the conspicuousness of ant–treehopper associations, it was investigated whether butterflies use them as visual cues for oviposition and, if so, which participants of the association are used as cues: ants, treehoppers, or both.4. Experiments using dried insects on paired branches revealed that females visually recognise ants and ant–treehopper associations, using them for egg‐laying decisions. However, presence of a treehopper aggregation alone had no effect on oviposition choices.5. This is a first insight into the importance of visual discrimination for ovipositing myrmecophilous butterflies. The results show that facultative mutualisms can be important enough to promote a behavioural adaptation (visual detection of ants) reinforcing the interaction. Our research highlights the importance of the behavioural interface within complex multispecies systems.

The cost of ant attendance and melezitose secretion in the black bean aphid Aphis fabae

1. The aphid Aphis fabae (Scopoli) is facultatively tended by Lasius niger (Linnaeus) ants. Previously, we found that A. fabae colonies can be made up of several clones, and that clones display significant differences in the composition of their honeydew sugars, especially in the amount of the ant attractant sugar melezitose that they produce.2. These clonal differences could greatly impact the strength of the mutualistic interaction with ants as well as the aphids' fitness.3. Hence, the aim of this study was to compare the fitness of different A. fabae clones that differed in their melezitose secretion, and whether or not they were tended by ants.4. Individual fitness indices, colony growth, and alate production of single‐clone aphid colonies were analysed.5. The results demonstrate that the fitness consequences of ant attendance critically depend on an interaction between levels of melezitose production. In particular, we show that high‐melezitose secreting clones produce fewer alates and hence might have a lower dispersal ability in the presence of ants.6. Furthermore, these data confirm previous evidence that ant attendance is costly and results in the production of fewer apterae.

Ant tending impairs performance of Aenasius bambawalei by manipulating the honeydew composition produced by Phenacoccus solenopsis

AbstractHoneydew produced by hemipterans is known as a possible kairomonal resource for parasitoids. The application of artificial honeydew effectively improves the performance of natural enemies. Aenasius bambawalei is a particularly dominant and aggressive endoparasitoid of the invasive mealybug Phenacoccus solenopsis. Our previous study showed that tending by the ghost ant Tapinoma melanocephalum significantly reduced the parasitism of A. bambawalei. We hypothesize that ghost ant tending influences host location of parasitoids by manipulating the composition of the honeydew produced by mealybugs. In this study, we tested whether the honeydew composition differs between treatments with and without ant attendance and whether changes in the honeydew influence the performance of A. bambawalei. Our results show that the sucrose concentration increased significantly in the ant‐attendance treatment but decreased when ant attendance was switched to an ant‐exclusion treatment; the inverse was true for the glucose concentration. Compared with the plastic honeydew treatment (mealybug with ant attendance), parasitoids spent much more time searching, had longer lifespans and showed higher parasitism on filter papers treated with natural honeydew (mealybug without any pre‐treatment) and those treated with convalescent honeydew (mealybug having experienced ant attendance and then switched to ant exclusion). These results support the hypothesis that ant tending influences the performance of parasitoids by manipulating honeydew composition.

Descriptiori of a grass feeding whitefly of the genusTetraleurodes(Hemiptera: Aleyrodidae) from the Indo-Myanmar border

A new species of whitefly, Tetraleurodes champaiensis Dubey sp. nov. (Hemiptera: Aleyrodidae) found infesting Sporobolus heterolepis (Poaceae) in Mizoram (India) is described along with measurements, line drawings and scanning electron microscope images. The species differs from Tetraleurodes thenmozhiae Jesudasan & David in being black in color and have bluntly pointed dorsal setae. The puparia of T. thenmozhiae are white and have capitate dorsal setae. The puparia of the new species were found feeding at the basal parts of central grass blades and almost near the ground level. An identification key to grass feeding Tetraleurodes species is provided. There was no ant attendance.

When a little means a lot – slight daily cleaning is crucial for obligatory ant-tended aphids

Ant-aphid mutualism has been investigated by many authors but it is unknown if anti-predator protection provided by ants is the main benefit for aphids. The aim of our paper is to analyse the ant-aphid interactions in the absence of predators. Based on video recordings we distinguish ant behaviours in interactions with attended aphids and we present ant time-budget at different times of the day. We also test if an aphid colony can survive without ant attendance in an environment free from predators and we inquire how much ant attendance is needed to maintain an aphid colony in good condition. Our study shows that, despite the lack of predation pressure, aphids of the species Cinara tujafilina were not able to survive without ant attendance and the extinction was caused by the excessive honeydew that covered aphids and their surroundings. We also found that ants cleaning aphids was the most frequent and time-consuming activity in ant-aphid interactions. However, in general, ants interacted with aphids only for less than 5% of their total time-budget. Thus, despite the fact that cleaning seems to be crucial in aphid survival, surprisingly little ant effort is needed to maintain an aphid colony in good condition.

Extrafloral nectary morphology and the role of environmental constraints in shaping its traits in a common Cerrado shrub (Maprounea brasiliensis A. St.-Hill: Euphorbiaceae)

This study aimed to elucidate the anatomy and morphology of extrafloral nectaries (EFNs) in Maprounea brasiliensis and whether environmental factors influence their traits of production and morphology. For this reason, we sampled leaves from individuals subjected to distinct fire and water regimes, and the anatomy and ultrastructures of EFNs as well as the chemical constitution of nectar were analyzed. EFN nectar production was associated with immature and recently expanded leaves. EFNs originate from the epidermis. At the end of ontogeny, secretory cells are surrounded by three or more layers of cells with secondary and lignified walls, isolating the EFN of vascular tissue. The ultrastructural analysis revealed mature EFNs with secretory activity. The experiments showed that EFN production was not influenced by the presence of frequent fires. However, during the rainy season, new produced leaves had nectaries in greater quantity and diameter than leaves produced during the dry season. The anatomical and ultrastructural changes demonstrated that nectar production is strongly influenced by the age of the nectaries which influence ant attendance to EFN since no ants were observed on leaves that did not secrete nectar. The seasonality experiment confirmed that EFNs of M. brasiliensis are resource dependent and evolutionary programed to appear in elevated number during the rainy season.

Alate production in an aphid in relation to ant tending and alarm pheromone

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate.2. Ant‐tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal.3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linné, 1758) ants.4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae.5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.

Multiple ant species tending lac insect Kerria yunnanensis (Hemiptera: Kerriidae) provide asymmetric protection against parasitoids.

This study investigated the effects of ant attendance on the parasitoid community and parasitism of lac insect Kerria yunnanensis aggregations in Yunnan province, China. We manipulated ant attendance to establish three treatments: (1) ant exclusion; (2) low ant attendance by several ant species; and (3) high ant attendance by Crematogaster macaoensis. Five parasitoid species were collected, with two species contributing 82.7 and 13.2% of total abundance respectively. Total parasitoid abundance was lowest in the February sample when K. yunnanensis was in its younger life stage, being significantly lower in the ant exclusion treatment. In April, all three treatments had significantly different parasitoid abundances, being highest in the ant exclusion treatment and the lowest in the high ant attendance treatment. When ants were present, there were strong negative relationships between total parasitoid abundance and ant abundance, with the relationships being dependent upon the ant species composition and abundance. The patterns of total parasitoid abundance were driven by the two most abundant parasitoid species. Parasitoid species richness did not differ among treatments or between sample times, however, multivariate analysis confirmed that overall parasitoid community structure differed significantly among treatments and between sample times, with the high ant attendance treatment differing most from the other two treatments. Interestingly the absence of ants did not result in increased parasitism from four of the five parasitoids. Ants in lac insect farming systems have a clear role for agricultural pest management. A full understanding of the asymmetric abilities of ants to influence parasitoid communities, and affect parasitism of hosts will require further experimental manipulation to assess the relative roles of 1) the abundance of each individual ant species on parasitoid access to hosts, 2) competition among parasitoids, and 3) the interaction between the first two factors.

Costs and constraints in aphid‐ant mutualism

AbstractWhile many studies have demonstrated that ants provide beneficial services to aphids, Bristow (Ant‐plant interactions, Oxford University Press, Oxford, 104–119, 1991) first questioned why so few aphid species are ant‐attended. Phylogenetic trees have demonstrated multiple gains and loss of ant‐attendance in the course of aphid‐ant interactions, implying that mutualisms easily form and dissolve. Several studies have reported the factors that influence the formation and maintenance of aphid‐ant interactions. Examples include the physiological costs of ant attendance, competition for mutualistic ants, ant predation on aphids, the influence of host plants, and parasitoid wasps. Recent physiological techniques have also revealed the chemical component of aphid‐ant mutualisms. The honeydew of ant‐attended aphids contains melezitose (a trisaccharide), which has an important role in aphid‐ant interactions. Studies of cuticular hydrocarbons on aphids and ants have clarified the underlying mechanisms of ant predation on aphids. Attending ants also reduce aphid dispersal ability, causing the formation of fragmented aphid populations with low genetic diversity in each population. The reduced aphid dispersal could be partly explained by higher wing loading and reduction of flight apparatus due to ant attendance. Whether ant attendance is associated with the range of host plants of aphids or genetic variation in microorganism in aphids remain to be explored.

Insect mutualisms buffer warming effects on multiple trophic levels

Insect mutualisms can have disproportionately large impacts on local arthropod and plant communities and their responses to climatic change. The objective of this study was to determine if the presence of insect mutualisms affects host plant and herbivore responses to warming. Using open-top warming chambers at Harvard Forest, Massachusetts, USA, we manipulated temperature and presence of ants and Chaitophorus populicola aphids on Populus tremuloides host plants and monitored ant attendance and persistence of C. populicola, predator abundance, plant stress, and abundance of Myzus persicae, a pest aphid that colonized plants during the experiment. We found that, regardless of warming, C. populicola persistence was higher when tended by ants, and some ant species increased aphid persistence more than others. Warming had negligible direct but strong indirect effects on plant stress. Plant stress decreased with warming only when both ants and C. populicola aphids were present and engaged in mutualism. Plant stress was increased by warming-induced reductions in predator abundance and increases in M. persicae aphid abundance. Altogether, these findings suggest that insect mutualisms could buffer the effects of warming on specialist herbivores and plants, but when mutualisms are not intact, the direct effects of warming on predators and generalist herbivores yield strong indirect effects of warming on plants.

Aphid Genotype Determines Intensity of Ant Attendance: Do Endosymbionts and Honeydew Composition Matter?

Abstract Ant—aphid interactions are well-studied mutualisms, but surprisingly, the intraspecific variation in the degree of ant attendance of aphids has been less appreciated than interspecific variation. Honeydew composition is a key factor in determining aphids' traits in relation to the intensity of ant attendance, and composition may be altered by endosymbiotic bacteria. Here, we evaluate relationships among the intensity of ant attendance, honeydew composition, and aphids' endosymbionts. We found differences in the intensity of ant attendance and endosymbiont composition between clones of cowpea aphids (Aphis craccivora Koch). To investigate whether aphid genotype, endosymbionts, or both, influence honeydew composition, and the relative influence of these factors on the intensity of ant attendance, a secondary symbiont of the aphid, Arsenophonus, was removed from the clone exhibiting a lower degree of ant attendance. Then, the sugar and amino acid composition of honeydew were compared between different aphid genotypes and between same genotype with and without Arsenophonus. The experiments demonstrated that there was a difference in the sugar composition of honeydew between clones, but that Arsenophonus did not influence this difference. Furthermore, the intensity of ant attendance of the clone did not change after removing Arsenophonus. These results suggest that variation in the degree of ant attendance of this aphid is caused by aphid genotype, not by endosymbionts.

Herbivore-constructed leaf shelters on Salix eriocarpa shoots affect arthropod communities

We observed the abundance of leaf shelters, aphids, other herbivores, and predators on willow trees, Salix eriocarpa, from May to October 2003. There was a positive correlation between the growth rate of aphids and the number of ants per shoot, suggesting ant attendance to aphids. Although the mean abundance of leaf shelters per shoot was rather low (1.7–2.2) throughout the observation period, aphids preferred to use shoots with leaf shelters compared with those without leaf shelters. The abundance of ants was positively influenced by the presence of leaf shelters and aphids from May to August. The abundance of other herbivores was positively influenced by leaf shelters, but negatively influenced by aphid presence from May to August. Furthermore, leaf shelters had a positive effect on the abundance of predators from July to October. These data suggest that a relatively low abundance of naturally occurring leaf shelters per shoot influenced the arthropod communities on S. eriocarpa, and the effect of those leaf shelters on each type of arthropod varied according to the season.

Do additional sugar sources affect the degree of attendance of Dysmicoccus brevipes by the fire ant Solenopsis geminata?

AbstractMutualistic interactions between ants and Hemiptera are mediated to a large extent by the amount and quality of sugar‐rich honeydew produced. Throughout the neotropics, the predaceous fire ant Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) is found in association with colonies of the pineapple mealybug, Dysmicoccus brevipes (Cockerell) (Hemiptera: Pseudococcidae), which they actively tend and protect from attack by natural enemies. In this study, we evaluate the effects of access to a sucrose solution on the mutualistic association between S. geminata and D. brevipes. Ten colonies of either species were established, with D. brevipes maintained on pumpkin, Cucurbita maxima Duchesne (Cucurbitaceae), in screen cages. Five of the S. geminata colonies were permitted access to vials with 20% sucrose solution and a pumpkin with 20 adult mealybugs. The remaining ant colonies were allowed access to mealybug‐infested pumpkins. Ant colonies with access to the sucrose solution attended mealybugs significantly less than those without additional sugar sources. Mealybug survival rates were similar under both treatments. Total body sugars and fructose were nearly twice as high in ants with access to honeydew and sucrose vs. those with access to honeydew and water. Fructose accumulated on the pumpkins over time in both treatments, suggesting that honeydew was not fully exploited by the ants. In conclusion, D. brevipes enjoy lower degrees of ant attendance when S. geminata have alternative sources of carbohydrates. We further discuss the significance of these findings for the conservation of predaceous ants and mealybug biological control.

Evaluation of the benefits of a myrmecophilous oribatid mite, Aribates javensis, to a myrmicine ant, Myrmecina sp.

I studied the myrmicine ant Myrmecina sp. A in West Java, Indonesia, which had the obligately myrmecophilous oribatid mite Aribates javensis in its nests. The oribatid mites cannot survive without ant attendance. The ants rarely eat living mites, but they feed on the mites in case of food shortage and after death of the mites. I examined the effects of the oribatid mites as food on the host ants. Egg production by ergatoid (i.e. permanently wingless) queens and larval survival of ant colonies, as well as survival and egg laying of isolated ant workers were investigated. The presence of oribatid mites had no effects on egg production by ergatoid queens and survival of the ant larvae neither in the presence of abundant food nor under starvation conditions. Survival of adult workers was not affected by the presence of oribatid mites, but egg production by workers was significantly enhanced by feeding on mites. The present results indicate that the oribatid mites had slight but significant nutritional effects on the host ants.

Sugar feeding of the common black ant, Lasius niger (L.), as a possible indirect method for reducing aphid populations on apple by disturbing ant-aphid mutualism

The rosy apple aphid, Dysaphis plantaginea Passerini, and the green apple aphid, Aphis pomi De Geer, are serious pests of apple and are commonly found together as pests in apple orchards. Both species establish mutualistic relationships with ants.Two experiments manipulating the presence of the common black ant, Lasius niger (L.), visiting aphid colonies by ant-exclusion with sticky barriers, or ant-feeding with honey as an alternative sugar source, were conducted, one in an apple orchard in the United Kingdom and one in an apple orchard in Hungary to test if these methods can reduce aphid infestations on apple trees.The exclusion of ants reduced D. plantaginea and A. pomi populations in both experiments. It caused significant increases in natural enemy pressure on both aphid species in the experiment in the UK and on A. pomi in the experiment in Hungary.Ant-feeding with honey reduced the numbers of ants tending D. plantaginea colonies, and it consequently resulted in a reduction in D. plantaginea populations in both experiments. The supplementary feeding of ants was more effective in reducing D. plantaginea than A. pomi. This was probably due to the greater intensity of ant attendance on A. pomi than on D. plantaginea colonies when both species were present together.Our results showed that supplementary sugar feeding of ants is a successful method for supporting biocontrol of apple aphids through enhancing the effectiveness of their natural enemies. However, the species of aphid targeted and the design and position of the feeder could affect the efficacy of this biocontrol method.

Myrmecophilous aphids produce cuticular hydrocarbons that resemble those of their tending ants

AbstractAphid‐tending ants protect aphids from natural enemies and collect honeydew secreted by the aphids. However, ants also often prey on the aphids they attend. Aphids, therefore, like social parasites of ants, may well have evolved chemical mimicry as an anti‐predation strategy. In this study, we aimed to determine whether the aphid Stomaphis yanonis actively produces cuticular hydrocarbons (CHCs) that resemble those of the tending ant Lasius fuji. In the wild, ants put their CHCs on the aphids that they are tending, so in this study we analyzed “ant‐free” aphids. Mature aphids that exuviated in the absence of ant attendance had almost all of the hydrocarbon components that the ants’ CHCs had. Moreover, hydrocarbons artificially applied to the aphids’ body surface were lost by exuviation. Taken together, these findings indicate that mature aphids actively produced ant‐like CHCs, and they constitute the first documentation of a chemical resemblance between aphids and ants in a specific aphid–ant association.

Reciprocally beneficial interactions between introduced plants and ants are induced by the presence of a third introduced species

Interspecific interactions play an important role in the success of introduced species. For example, the ‘enemy release’ hypothesis posits that introduced species become invasive because they escape top–down regulation by natural enemies while the ‘invasional meltdown’ hypothesis posits that invasions may be facilitated by synergistic interactions between introduced species. Here, we explore how facilitation and enemy release interact to moderate the potential effect of a large category of positive interactions – protection mutualisms. We use the interactions between an introduced plant (Japanese knotweed Fallopia japonica), an introduced herbivore (Japanese beetle Popillia japonica), an introduced ant (European red ant Myrmica rubra), and native ants and herbivores in riparian zones of the northeastern United States as a model system. Japanese knotweed produces sugary extrafloral nectar that is attractive to ants, and we show that both sugar reward production and ant attendance increase when plants experience a level of leaf damage that is typical in the plants’ native range. Using manipulative experiments at six sites, we demonstrate low levels of ant patrolling, little effect of ants on herbivory rates, and low herbivore pressure during midsummer. Herbivory rates and the capacity of ants to protect plants (as evidenced by effects of ant exclusion) increased significantly when plants were exposed to introduced Japanese beetles that attack plants in the late summer. Beetles were also associated with greater on‐plant foraging by ants, and among‐plant differences in ant‐foraging were correlated with the magnitude of damage inflicted on plants by the beetles. Last, we found that sites occupied by introduced M. rubra ants almost invariably included Japanese knotweed. Thus, underlying variation in the spatiotemporal distribution of the introduced herbivore influences the provision of benefits to the introduced plant and to the introduced ant. More specifically, the presence of the introduced herbivore converts an otherwise weak interaction between two introduced species into a reciprocally beneficial mutualism. Because the prospects for facilitation are linked to the prospects for enemy release in protection mutualisms, species introductions can have complex effects on existing species interactions, between both native and introduced species.

The Effect of Ants on the Population Dynamics of a Protective Symbiont of Aphids, Hamiltonella defensa

Abstract Mutualists that provide redundant services to the same organism have been shown both to coexist and compete for access to the partner. Aphids, for example, are known to receive protection against natural enemies from both heritable bacterial symbionts as well as ants, which tend aphids in exchange for sugary honeydew excretions. Little is known, however, about how ant attendance might influence interactions between aphids and their protective bacteria. Assuming costs to infection, we hypothesized that protective symbiont prevalence would decrease in the presence of ants, because of duplication of services. We surveyed natural aphid populations and found Hamiltonella defensa, a bacterium that provides resistance to aphids against parasitoid wasps in laboratory settings, among several aphid species, including Obtusicauda frigidae (Oestlund 1886). We excluded ants from protecting O. frigidae aggregations and measured the effect of ant absence on the frequency of parasitoid attack and H. defensa infection in aphid groups. Ant presence did not reduce H. defensa frequency in aphids, likely because ants and H. defensa did not significantly lower parasitoid wasp attack rates. Metabolic costs likely control H. defensa prevalence more than the effect of ant-tending.

Seasonal changes in the flight apparatus of winged females and sexual males of the aphid Tuberculatus quercicola (Hemiptera: Aphididae)

Tuberculatus quercicola (Matsumura) feeds on Quercus dentata Thunberg, and has mutualistic interactions with ants. Tuberculatus quercicola has two winged morphs in its life cycle, winged females appear in summer and sexual males appear in autumn. Previous studies have shown that wing loading (ratio of body volume to wing area) is higher for the winged females, because of ant attendance, resulting in extremely low dispersal. It is known that the nutritional quality of host plants is high in spring and autumn, when leaves are growing or senescent, and low in summer when leaves are mature. This study examined the effects of seasonal plant deterioration on the development of flight apparatus (wing size and flight muscle) of winged females and males. Moreover, field intercept traps were used to examine the extent of dispersal of males. The results showed that seasonal plant deterioration affected development of the flight apparatus of winged females, particularly flight muscle. Flight muscle development was significantly higher in winged males in autumn than in winged females. However, winged males were not caught in any of the traps. The different resource allocation to the flight apparatus of winged females and males is discussed.

The aphid‐tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons

AbstractSome aphid species are attended by ants, which protect aphids against enemies, but ants sometimes prey on the aphids they are attending depending on the resource conditions. A previous study indicated that the ant Lasius niger preys less on the aphid individuals that experienced ant attendance than on those that did not. This observation leads to the hypothesis that ants transfer some substances to the aphids they attend and selectively prey on the aphids without the substances. In this study, we focus on cuticular hydrocarbons (CHCs), which are used by ants as nestmate recognition substances, and test whether ants discriminate the aphids on the basis of CHCs. We confirmed that the ant Lasius fuji preyed less on the aphids that were attended by their nestmates than those that were not attended. Glass dummies treated with CHCs from attended aphids were attacked less by ants than those treated with CHCs from non‐attended aphids. The CHC profiles of ant attended aphids resembled those of the ants, suggesting that ants’ CHCs are transferred to the aphids’ body surface through ant attendance. These results support the hypothesis that ants “mark” their attended aphids with their CHCs and the CHCs reduce ant predation intensity.