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.     

Comparing wing loading,flight muscle and lipid content in ant‐attended and non‐attended Tuberculatus aphid species

Although all Tuberculatus aphids possess wings, some species associated with ants exhibit extremely low levels of dispersal compared with those not associated with ants. Furthermore, phylogenetic interspecific comparisons find significantly higher wing loading (i.e. higher ratio of body volume to wing area) in ant‐attended species. This observation indicates that ant‐attended species may allocate more of their body resources to reproductive traits (i.e. embryos) rather than flight apparatus (i.e. wings, flight muscle and lipid). The present study focuses on two sympatric aphid species and aims to investigate the hypothesized trade‐off in resource investment between fecundity and the flight apparatus; specifically, the ant‐attended Tuberculatus quercicola (Matsumura) and non‐attended Tuberculatus paiki Hille Ris Lambers. Species differences are compared in: (i) morphology, (ii) embryo production, (iii) triacylglycerol levels and (iv) wing loading and flight muscle. The results show that T. quercicola has a larger body volume, higher fecundity and higher wing loading compared with T. paiki, which has a smaller, slender‐shaped body, lower fecundity and lower wing loading. No significant difference is found between the species with respect to the percentage of triacylglycerol content in dry body weight. The flight muscle development is significantly lower in T. quercicola than in T. paiki. These results indicate that the additive effect of higher wing loading and the lower amount of flight muscle development in T. quercicola may increase the physical difficulty of flight, and hence be responsible for its lower dispersal ability. The trade‐off between fecundity and dispersal documented in wing‐dimorphic insects may therefore be applicable to T. quercicola, which has fully developed wings.     

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.     

Ant semiochemicals limit apterous aphid dispersal

Some organisms can manipulate the nervous systems of others or alter their physiology in order to obtain benefit. Ants are known to limit alate aphid dispersal by physically removing wings and also through chemical manipulation of the alate developmental pathway. This results in reduced dispersal and higher local densities of aphids, which benefit ants in terms of increased honeydew and prey availability. Here, we show that the walking movement of mutualistic apterous aphids is also reduced by ant semiochemicals. Aphids walk slower and their dispersal from an unsuitable patch is hampered by ants. If aphid walking dispersal has evolved as a means of natural enemy escape, then ant chemicals may act as a signal indicating protection; hence, reduced dispersal could be adaptive for aphids. If, however, dispersal is primarily a means to reduce competition or to maintain persistent metapopulations, then manipulation by ants could be detrimental. Such manipulation strategies, common in host-parasite and predator-prey interactions, may be more common in mutualism than expected.     

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.     

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.     

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.     

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.     

Seasonal changes in the flight apparatus of winged females and sexual males of the aphid <Emphasis Type="Italic">Tuberculatus quercicola</Emphasis> (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.     

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.     

Do aphids actively search for ant partners?

The aphid–ant mutualistic relationships are not necessarily obligate for neither partners but evidence is that such interactions provide them strong advantages in terms of global fitness. While it is largely assumed that ants actively search for their mutualistic partners namely using volatile cues; whether winged aphids (i.e., aphids’ most mobile form) are able to select ant‐frequented areas had not been investigated so far. Ant‐frequented sites would indeed offer several advantages for these aphids including a lower predation pressure through ant presence and enhanced chances of establishing mutuaslistic interactions with neighbor ant colonies. In the field, aphid colonies are often observed in higher densities around ant nests, which is probably linked to a better survival ensured by ants’ services. Nevertheless, this could also result from a preferential establishment of winged aphids in ant‐frequented areas. We tested this last hypothesis through different ethological assays and show that the facultative myrmecophilous black bean aphid, Aphis fabae L., does not orientate its search for a host plant preferentially toward ant‐frequented plants. However, our results suggest that ants reduce the number of winged aphids leaving the newly colonized plant. Thus, ants involved in facultative myrmecophilous interactions with aphids appear to contribute to structure aphid populations in the field by ensuring a better establishment and survival of newly established colonies rather than by inducing a deliberate plant selection by aphid partners based on the proximity of ant colonies.     

Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers

Interaction between a predator and a parasitoid attacking ant-attended aphids was examined in a system on photinia plants, consisting of the aphid Aphis spiraecola, the two ants Lasius japonicus and Pristomyrmex pungens, the predatory ladybird beetle Scymnus posticalis, and the parasitoid wasp Lysiphlebus japonicus. The ladybird larvae are densely covered with waxy secretion and are never attacked by attending ants. The parasitoid females are often attacked by ants, but successfully oviposit by avoiding ants. The two ants differ in aggressiveness towards aphid enemies. Impacts of the predator larvae and attending ant species on the number of parasitoid adults emerging from mummies per aphid colony were assessed by manipulating the presence of the predator in introduced aphid colonies attended by either ant. The experiment showed a significant negative impact of the predator on emerging parasitoid numbers. This is due to consumption of healthy aphids by the predator and its predation on parasitized aphids containing the parasitoid larvae (intraguild predation). Additionally, attending ant species significantly affected emerging parasitoid numbers, with more parasitoids in P. pungens-attended colonies. This results from the lower extent of interference with parasitoid oviposition by the less aggressive P. pungens. Furthermore, the predator reduced emerging parasitoid numbers more when P. pungens attended aphids. This may be ascribed to larger numbers of the predator and the resulting higher levels of predation on unparasitized and parasitized aphids in P. pungens-attended colonies. In conclusion, a negative effect of the predator on the parasitoid occurs in ant-attended aphid colonies, and the intensity of the interaction is affected by ant species.     

The impact of ant attendance on protecting <Emphasis Type="Italic">Aphis gossypii</Emphasis> against two aphidophagous predators and it’s role on the Intraguild Predation between them

In this study the changes in Aphis gossypii Glover populations tended by the homopteran- tending ant, Tapinoma simrothi Krausse when exposed to the natural enemies Chrysoperla carnea Stephens and Coccinellia septempunctata Mulsant was studied. We also studied the effect of ant’s attendance on the consequence of intraguild predation (IGP) between these two predators. The presence of ants T. simrothi had deterrent impact on natural enemies of A. gossypii compared to control aphid populations in absence of ants. Equally we observed that IGP between two aphid predators decreased when T. simrothi was present. The lowest IGP level was observed when both aphids and ants were present in the microcosm arena. In the microcosm arena the presence of ants had an indirect effect on the occurrence of IGP. Our results suggest that although the mutualistic ants have an indirect impact on the IGP by aphidophages predators, but their roles should not be ignored.     

Today and tomorrow: impact of climate change on aphid biology and potential consequences on their mutualism with ants

Recent studies about mutualism consider the complexity and versatility of the relationship, in addition to highlighting the importance of the cost/benefit balance between the two protagonists. Because species interactions are highly dependent on the environment, the climate changes foreseen for the coming years are expected to have significant impacts on the evolution of mutualistic interactions. Among mutualisms, the aphid–ant interaction is well documented, partly explained by the pest status of aphids. This literature review focuses on the impact of climate change (particularly atmospheric carbon dioxide concentration and temperature) on aphid biology and the potential consequences with respect to their mutualistic interactions with ants. We provide an overview of the published reports concerned with the effects of temperature and carbon dioxide on aphids, for which a positive, a negative or no effect has been highlighted. We then discuss how climatic changes can alter four major components of aphid biology that are shaping their interaction with ants: (i) aphid population growth; (ii) aphid behaviour and mobility; (iii) honeydew production and composition; and (iv) semiochemistry. Finaly, we discuss the limitations of such studies on aphid–ant mutualism, as well as the information that is still needed to predict how climate change might impact this type of relationship.     

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.     

Role of ants in structuring the aphid community on apple

1. The aphids Dysaphis plantaginea Passerini, Aphis spp. (Aphis pomi De Geer and Aphis spiraecola Patch), and Eriosoma lanigerum Hausmann are commonly found together in apple orchards. Ants establish a mutualistic relationship with the myrmecophilous aphids D. plantaginea and Aphis spp. but not with E. lanigerum. 2. Field surveys and one experiment manipulating the presence of ants and the aphid species were conducted to test the hypothesis that ants play a role in structuring the community of these aphids on apple. 3. Ants tended D. plantaginea and Aphis spp. but not E. lanigerum colonies. In the field, D. plantaginea performed better in the presence of ants while no effect was observed in Aphis spp. Contrarily, populations of Aphis spp. in the manipulative experiment performed better in the presence of ants while no differences were observed for D. plantaginea. Such differences between field and manipulative conditions could be related to thermal tolerance, phenology, and life cycles. In contrast, populations of E. lanigerum were reduced in the presence of ants. 4. Ants also had a significant negative effect on the abundance of natural enemies, which could partially explain the benefits to the tended aphids. However, while ants did not provide a benefit to Aphis spp. when it was reared alone, in the presence of other species ant attendance increased Aphis abundance by 256% and simultaneously reduced E. lanigerum abundance by 63%. Therefore, ants benefited Aphis by reducing competition with other aphid species, which involves a different mechanism, explaining the benefit of ant attendance. Considering all the aphid species together, ants had a net positive effect on aphid abundance, which was consequently considered harmful for the plant. 5. Our results highlighted the role that ants play in structuring apple aphid communities and give support to the observed pattern that ants can benefit tended aphids while simultaneously reducing the abundance of untended herbivores.     

How an ant decides to prey on or to attend aphids

The following results on the behavior decision making of the antLasius niger toward two species of myrmecophilous aphidsLachnus tropicalis andMyzocallis kuricola on chestnut trees have been found. (1) An individual worker consistently attended only one aphid species, even if her nestmates attended other aphid species on the same tree. (2) The ants preyed less on the aphid species which they attended than on other myrmecophilous aphid species. (3) The ants preyed less on the aphids which had been attended by their nestmates, even if both aphids were the same species. (4) The ants preyed less on aphids which had provided honeydew to their nestmates. (5) The increased aphid density per ant led to an increase in the rate of predation on the introduced aphids by the ants. These results suggest that each worker ofL. niger chooses aphid species to attend from her experience. In addition, the workers can recognize whether an aphid has been attended by their nestmates and whether an aphid has given their nestmates honeydew. Through these processes, each worker decides to attend or to prey on the aphid. As a result, they may realize efficient collective foraging dependent on aphid density per worker.     

Plant genotype shapes ant-aphid interactions: implications for community structure and indirect plant defense

Little is known about the mechanisms by which plant genotype shapes arthropod community structure. In a field experiment, we measured the effects of milkweed (Asclepias syriaca) genotype and ants on milkweed arthropods. Populations of the ant-tended aphid Aphis asclepiadis and the untended aphid Myzocallis asclepiadis varied eight- to 18-fold among milkweed genotypes, depending on aphid species and whether ants were present. There was no milkweed effect on predatory arthropods. Ants increased Aphis abundance 59%, decreased Myzocallis abundance 52%, and decreased predator abundance 56%. Milkweed genotype indirectly influenced ants via direct effects on Aphis and Myzocallis abundance. Milkweed genotype also modified ant-aphid interactions, influencing the number of ants attracted per Aphis and Myzocallis. While ant effects on Myzocallis were consistently negative, effects on Aphis ranged from antagonistic to mutualistic among milkweed genotypes. As a consequence of milkweed effects on ant-aphid interactions, ant abundance varied 13-fold among milkweed genotypes, and monarch caterpillar survival was negatively correlated with genetic variation in ant abundance. We speculate that heritable variation in milkweed phloem sap drives these effects on aphids, ants, and caterpillars. In summary, milkweed exerts genetic control over the interactions between aphids and an ant that provides defense against foliage-feeding caterpillars.     

Ant–aphid mutualism: the influence of ants on the aphid summer cycle

There are few longtime studies on the effects on aphids of being tended by ants. The aim of this study is to investigate how the presence of ants influences settling decisions by colonizing aphids and the post‐settlement growth and survival of aphid colonies. We conducted a field experiment using the facultative myrmecophile Aphis fabae and the ant Lasius niger. The experiment relied on natural aphid colonization of potted plants of scentless mayweed Tripleurospermum perforatum placed outdoors. Ants occurred naturally at the field site and had access to half of the pots and were prevented from accessing the remainder. The presence of winged, dispersing aphids, the growth and survival of establishing aphid colonies, and the presence of parasitoids were measured in relation to presence or absence of ants, over a period of five weeks. The presence of ants did not significantly influence the pattern of initial host plant colonization or the initial colony growth, but ant‐tended aphids were subject to higher parasitism by hymenopteran parasitoids. The net result over the experimental period was that the presence of ants decreased aphid colony productivity, measured as the number of winged summer migrants produced from the colonized host plants. This implies that aphids do not always benefit from the presence of ants, but under some conditions rather pay a cost in the form of reduced dispersal.