Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola

The defensive effects of ants against aphid predators have been well documented in the mutualistic relationship of aphids and their attending ants. However, it is not clear whether ant attendance has any direct effect on the aphids' growth and reproduction. Through field experiments, this study evaluates the benefits and, in particular, the costs of ant attendance to aphid colonies, focusing on the drepanosiphid aphid Tuberculatus quercicola which is associated with the Daimyo oak, Quercus dentata , and which is always attended by the red wood ant Formica yessensis . Ant attendance was clearly beneficial to the aphid; the exclusion of ants led to a significant increase in the extinction rate of aphid colonies. However, MANOVA and randomized block ANOVA indicated that in colonies continuously attended by ants, aphids had significantly smaller body size and produced a smaller number of embryos than in colonies isolated from ants when they were reared under homogeneous host conditions free from natural enemies. Thus, ant attendance had a negative influence on the growth and reproduction of the aphids, even though it contributed to the greater longevity of the aphid colonies. We hypothesize that ant-attended aphids are under intense selective pressures that act against aphid clones which fail to attract many ants, so that aphids have developed an adaptive mechanism to allocate a larger fraction of resources to the honeydew when they are requested to do so by the ants in order to ensure the ants' consistent visitation.     

Costs and constraints in aphid-ant mutualism

While 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.     

Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola

Abstract 1. Mutualistic interactions between aphids and ants are mediated by honeydew that aphids produce. Previous work showed that when attended by the ant Formica yessensis Forel (Hymenoptera: Formicidae), nymphs of the aphid Tuberculatus quercicola (Matsumura) (Homoptera: Aphididae) developed into significantly smaller adults with lower fecundity than did nymphs that were not ant attended.
2. This study tested the hypothesis that this cost of ant attendance arises through changes in the quality and quantity of honeydew. Ant-attended and ant-excluded aphid colonies were prepared in the field. The composition and concentration of amino acids were compared between the honeydew produced by ant-attended colonies and that produced by ant-excluded colonies.
3. The aphids excreted smaller droplets of honeydew, but also excreted them more frequently, in ant-attended colonies than in ant-excluded colonies. The honeydew of ant-attended aphids contained more types of amino acid, and a significantly higher total concentration of amino acids, than did the honeydew of ant-excluded aphids.
4. These results suggest that the increase in the concentration of amino acids in honeydew leads to a shortage of nitrogen available for aphid growth and reproduction, resulting in lower performance under ant attendance.
5. With the advance of seasons, a significant reduction was found in both the total free amino acid concentration in phloem sap and the frequency of honeydew excretion; however the total concentration of amino acids in the honeydew did not vary significantly during the seasons, suggesting that aphids keep the quality of honeydew constant in order to maintain ant visitation.     

A comparative analysis of morphological and ecological characters of European aphids and lycaenids in relation to ant attendance

Ants are a major environmental factor for many insect species. For example, aphids and lycaenids have evolved an array of associations with ants ranging from obligate myrmecophily to the avoidance of contact. Here we (1) analyze the predictive power of different ecological and morphological traits for explaining the strength of the association between ants and aphids/lycaenids and (2) contrast different taxonomic levels with respect to the variance explained by ant attendance. Data come from a literature survey including 112 species of aphids and 103 species of lycaenids from Europe. For aphids, feeding on woody plant parts is positively associated with ant attendance, while a high degree of mobility, feeding in isolation, and the possession of wings in the adult stage are negatively associated with ant attendance. In lycaenids, feeding on inflorescences and feeding on Fabaceae host plants is closely associated with ant attendance, while living in forests bears a smaller likelihood to establish mutualistic relationships. Body size always appeared to be a poor predictor for the degree of ant attendance. Overall, in both insect groups less than 10% of the variation in the ecological traits recorded is explained by the different modes of ant association. When decomposing the variance in traits explained by ant attendance at different taxonomic levels, aphids and lycaenids show contrasting results. In aphids, most variance in the degree of ant attendance is explained at the subfamily level and least at the species level. The opposite is true for lycaenids, where most variance is explained at the lowest taxonomic level. Possible mechanisms explaining these different patterns of associations with ants are suggested.     

Ants andPolyommatus icarus immatures (Lycaenidae) —sex-related developmental benefits and costs of ant attendance

Summary Third and fourth instar larvae and pupae of the facultatively myrmecophilous Palaearctic blue butterflyPolyommatus icarus showed no alteration in developmental time when reared in the presence of two species ofLasius ants. Sex differences were observed in larval growth and pupal weight, with males growing larger and faster. Sex-related differences also occurred in the costs and benefits of ant-attendance. Male pupal masses tended to be larger in individuals associated with ants, and their pupal weight loss was not enhanced by ant attendance. This positive developmental effect of myrmecophily is tentatively attributed to a stimulating influence of ants on caterpillar feeding behavior. In contrast, females associated with ants tended to lose more weight during the pupal stage. Hence there is evidence for developmental benefits, rather than costs, of myrmecophily in maleP. icarus immatures, whereas ant attendance appears to be more costly for females during the pupal stage. These findings are discussed in relation to data on other myrmecophilous lycaenid species. It is suggested that maintaining low-level myrmecophily and its related organs is a comparatively inexpensive evolutionary stable strategy among this butterfly group.     

Cornicle length in Macrosiphini aphids: a comparison of ecological traits

Abstract 1. Aphids often emit cornicle droplets when attacked by predators. While the function of cornicle droplets has long been debated (i.e. mechanical protection vs. chemical signalling), it is not understood why aphid species have cornicles of different lengths.
2. It was hypothesised that aphids living in more scattered colonies have longer cornicles to scent-mark predators with cornicle droplets containing alarm pheromone, so that clone-mates are provided with advanced warning of a threat, even if not at the predation site. To test this hypothesis, multiple regression analyses were used, due to a lack of phylogenetic information on these taxa, to address which ecological traits (amount of wax on an aphid, degree of colony aggregation, feeding shelter, ant attendance) are correlated with cornicle length.
3. Aphids living in dense colonies tended to have shorter cornicles than aphids living in more scattered colonies. Also, aphids with more protection (i.e. wax) on their bodies had shorter cornicles. Aphids also tended to have shorter cornicles when tended by ants. The presence of a feeding shelter was not a good predictor of cornicle length.
4. It is suggested that longer cornicles function to scent-mark predators with alarm pheromone to increase the inclusive fitness of a clone; however the negative correlation between the amount of individual protection, and also ant attendance, and cornicle length argues for a trade-off between different forms of defence.     

Ant attendance reduces flight muscle and wing size in the aphid Tuberculatus quercicola

In otherwise mutualistic relationships between aphids and ants, attendance by ants often has negative impacts on aphids. For example, in a previous study using traps in the field, the aphid Tuberculatus quercicola, which exhibits mutualistic interactions with ants, showed extremely low dispersal rates, despite having long wings. This study investigates whether components of the flight apparatus (mesonotum length, flight muscle and wings) differ between aphids attended by ants and not attended by ants. Randomized block analysis of variance, using body length as a covariate, showed that ant attendance has a negative influence on aphid flight apparatus. This result indicates that aphids produce honeydew at the expense of resource investment in flight apparatus. Since the dispersal of T. quercicola is limited under ant attendance, the reduction in flight apparatus could precede a decrease in body size. This study also showed that flight apparatus was more developed in aphids under ant-exclusion conditions. This may imply that T. quercicola fly when ants are not available. The maintenance of flight apparatus in T. quercicola might therefore be partly explained by gene flow on the rare occasions that this aphid species disperses.     

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

Some 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.     

What determines conditionality in ant–Hemiptera interactions? Hemiptera habitat preference and the role of local ant activity

Abstract.  1. This paper describes spatial variation in density of a mutualist Hemiptera, and attempts to elucidate an understanding of the spatial variation in conditionality of its mutualism with ants.
2. Aggregations of the membracid treehopper, Campylenchia sp., occurred more frequently, and with higher number of individuals, in isolated trees as compared with their occurrence in the same tree species in wooded patches.
3. Using treehopper aggregations as the level of replication, there was a habitat × ant presence interaction associated with colony survival time. However, when the median survival time of all aggregations within each tree was used, only an additive effect of both habitat type and ant presence were apparent. This suggests that treehopper aggregations in some isolated trees experienced more benefit from ant presence than other trees.
4. The ant:treehopper ratio averaged over each tree was correlated with effect of ant presence on survivorship (survival time without ants/survival time with ants). Therefore, conditionality in the ant–membracid mutualism appears related to ant attendance level at the scale of individual trees.
5. Ant attendance at treehopper aggregations in isolated and matorral trees did not differ, and therefore there is no clear mechanism by which ants create the contrast in treehopper densities between the two habitat types.
6. The main force shaping initial treehopper densities in the two habitats is likely plant quality. Results suggest that growing situation (or more specifically plant health) is likely a good predictor of membracid density, while general ant activity within a tree is the best indicator of interaction strength.     

Seasonal changes in the response of wood-ants (Formica lugubris) to sucrose baits

Abstract. 1. The acceptability of sucrose solutions to Formica lugubris Zett. in the field was tested by offering droplets of known concentrations to ants tending aphids.
2. A probit model fitted to the data allowed the computation of the Median Effective Concentration (ED₅₀) and its confidence limits.
3. In spring and early summer ED₅₀ was about 0.15 M sucrose, but the ED₅₀ rose in 1 week at the end of June from 0.2 M to 0.9 M. The change was simultaneous on pine and birch trees. The ED₅₀ fell gradually to about 0.4 M in early November.
4. The increase in ED₅₀ is related to the production of the summer apterae in the aphids tended, Cinara pini (L.) on pines and Symydobius oblongus (von Heyden) on birch. This increases the 'quality' of food resource so that low sucrose concentrations can no longer compete for ant attendance.
5. The increase in ED₅₀ may limit the attendance of wood-ants at the nectaries of bracken, Pteridium aquilinum (L.) Kuhn. and at colonies of some other aphid species which are attended only in early summer.     

Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance

Abstract.  1. The population abundance and age structure of Rhopalosiphum padi , one of the most common maize aphid species, on transgenic Bt (expressing the Cry1Ab protein) and non-Bt isogenic maize was studied in commercial plots during three crop seasons.
2. A higher density of aphids, particularly alates and young nymphs, occurred in Bt plots at very young maize development stages, corresponding to the settlement period, in the 3 years studied. Possible causes are discussed. After this period, there were no differences between Bt and non-Bt maize.
3. Mortality, development, and reproduction of the offspring of alate forms of R. padi and the offspring of different generations of apterous forms fed with Bt maize were evaluated in the laboratory under controlled conditions.
4. The developmental and pre-reproductive times of the offspring of the first generation of alatae were shorter and the intrinsic rate of natural increase ( r _m ) higher when aphids fed on Bt maize. The opposite occurs with the offspring of the first generation of apterous mothers, which have lower nymphal and adult mortality, shorter developmental and pre-reproductive times, a higher effective fecundity rate, and greater r _m , when fed on non-Bt maize. The differences in aphid development on the two cultivars may be linked to changes in host-plant quality due to pleiotropic effects of the genetic modification.
5. No differences on aphid mortality, developmental and pre-reproductive times, fecundity, and r _m were found between the offspring of apterous aphids maintained on Bt or non-Bt maize for several generations.     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.     

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.     

The numbers and distribution of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.)

Abstract. 1. Subterranean aphids in old pasture were found to show extremely clumped distributions with about 3000 aphids (omitting first instars) per ant nest throughout the year.
2. They were generally distributed in and away from the nest mounds, but within the ant's foraging territories.
3. At summer temperatures, more than 3000 first instars are lost from the aphid population per ant nest per day and it is concluded that these are eaten by the ants in addition to some older aphids and the honeydew produced.
4. The aphids may therefore provide enough food to maintain the ants with very little extra needed in the form of other prey.     

Aphid-mediated coexistence of ladybirds (Coleoptera: Coccinellidae) and the wood ant Formica rufa: seasonal effects, interspecific variability and the evolution of a coccinellid myrmecophile.

It is generally believed that most homopteran-eating insects avoid ant-tended colonies of Homoptera, due to the ant aggression they encounter there. However, because homopteran colonies which are ant-tended often persist for longer than untended colonies, some homopteran-eaters may utilise ant-tended Homoptera when untended colonies are scarce. Furthermore, a few homopteran-eaters are myrmecophilous, habitually coexisting with ants. To investigate these phenomena, a study was made of aphids and aphidophagous coccinellids (ladybirds) on Scots pine, Pinus sylvestris , growing in areas foraged and unforaged by the wood ant Formica rufa . The non-tended aphid Schizolachnus pineti exhibited a marked population decline in late summer but persisted in both areas at very low density. Facultatively tended Cinara aphids exhibited higher population densities when associated with F. rufa , and remaining colonies of these aphids were only found associated with ants in late summer. Coccinellids exhibited considerable interspecific variability in their level of association with F. rufa , and there was some evidence of an increase in certain species' frequencies of occurrence with the ant when Cinara aphids were all ant-tended, in late summer. Coexistence with ants appears to be associated with either an intolerance of low aphid densities, in Coccinella septempunctata and Harmonia quadripunctata , or with extreme dietary specialisation, in Myzia oblongoguttata . Similar factors to those which bring C. septempunctata into contact with ants were probably of importance in the initial stages of the evolution of myrmecophily of its congener, Coccinella magnifica .     

Relative fitness of aphids: effects of plant quality and ants

We investigated the response of four species of aphids ( Metopeurum fuscoviride , Brachycaudus cardui , Aphis fabae , and Macrosiphoniella tanacetaria ) on tansy ( Tanacetum vulgare ) to plant quality and attendance by an ant, Lasius niger . The aphids experienced one of four different environments for two consecutive generations. Ant-attendance significantly affected the time needed to reach maximum fecundity only in Me. fuscoviride and plant quality in Me. fuscoviride and B. cardui . Maximum daily fecundity was positively affected by plant quality and the magnitude of the effect was inversely associated with the degree of myrmecophily. Ant-attendance had a positive effect on maximum fecundity only in the obligate myrmecophile, Me. fuscoviride . The intrinsic rate of population increase, r _m, on high quality plants, was lowest for the obligate myrmecophile, intermediate for the facultative myrmecophiles and highest for the unattended species. On high quality plants the fitness of Me. fuscoviride was more adversely affected by the developmental stage of the plant and absence of ants than that of A. fabae or Ma. tanacetaria , which were able to maintain a high relative fitness in all the environments. The implications for aphids experiencing different degrees of ant-attendance and seasonal changes in plant quality are discussed.     

The distribution of aphids in response to variation among individual host plants: Uroleucon rudbeckiae (Homoptera: Aphididae) andRudbeckia laciniata (Asteraceae)

Abstract. 1. An investigation was conducted to determine the effects of variation among individual plants of Rudbeckia laciniata L. on the distribution and abundance of the aphid Uroleucon rudbeckiae (Fitch).
2. Wild plants were examined repeatedly for up to 2¹/₂ years to obtain information about plant growth and flowering, and about aphid densities on individual plants.
3. Aphid densities on individual plants were positively associated with several measures of plant vigour, including height, growth since previous year, and occurrence of flowers.
4. The colonization of plants by alate aphids was more highly correlated with plant height than with plant exposure. Aphid densities on individual plants were more strongly associated with plant height than with number of colonists.
5. In all years there were many hosts which were never colonized by aphids. Some of these plants produced shoots but did not flower. Experimental infestation of these plants showed that they were unsuitable for aphid growth and reproduction. Some plants which did flower and which escaped aphid infestation were nevertheless suitable hosts. Previously unsuitable host individuals were able to support aphids when grown under glass-house conditions.     

Reproduction and dispersal in an ant-associated root aphid community

Clonal organisms with occasional sex are important for our general understanding of the costs and benefits that maintain sexual reproduction. Cyclically parthenogenetic aphids are highly variable in their frequency of sexual reproduction. However, studies have mostly focused on free‐living aphids above ground, whereas dispersal constraints and dependence on ant‐tending may differentially affect the costs and benefits of sex in subterranean aphids. Here, we studied reproductive mode and dispersal in a community of root aphids that are obligately associated with the ant Lasius flavus. We assessed the genetic population structure of four species (Geoica utricularia, Tetraneura ulmi, Forda marginata and Forda formicaria) in a Dutch population and found that all species reproduce predominantly if not exclusively asexually, so that populations consist of multiple clonal lineages. We show that population viscosity is high and winged aphids rare, consistent with infrequent horizontal transmission between ant host colonies. The absence of the primary host shrub (Pistacia) may explain the absence of sex in three of the studied species, but elm trees (Ulmus) that are primary hosts of the fourth species (T. ulmi) occurred within a few km of the study population. We discuss the extent to which obligate ant‐tending and absence of primary hosts may have affected selection for permanent parthenogenesis, and we highlight the need for further study of these aphids in Southern Europe where primary hosts may occur close to L. flavus populations, so that all four root aphid species would have realistic opportunities for completing their sexual life cycle.     

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

Aphid-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.     

Timing of dispersal: effect of ants on aphids

Mutualists can affect many life history traits of their partners, but it is unclear how this translates into population dynamics of the latter. Ant–aphid associations are ideal for studying this question, as ants affect aphids, both positively (e.g., protection against natural enemies) and negatively (e.g., reduction of potential growth rates). The unresolved question is whether these effects, which have been observed at the level of individuals and under controlled environmental conditions, have consequences at the population level. On estimating aerial aphid populations by using weekly suction trap data spanning up to 22 years from different locations in France, we show that in ant-attended aphid species long-distance dispersal occurs significantly later, but that the year-to-year changes in the peak number of migrants are not significantly lower than for non-attended aphids. Host alternation had the same retarding effect on dispersal as ant attendance. We discuss the delay in the timing of dispersal in ant-attended aphids, and potential costs that arise in mutualistic systems.