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.     

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.     

Competition hierarchies among ants and predation by birds jointly determine the strength of multi‐species ant–aphid mutualisms

Protection mutualisms often involve multiple species of protector that vary in quality as mutualists. Because protectors may compete for access to mutualists, concordance between competitive ability and degree of benefit will determine the overall strength of multi‐species mutualisms. We compared the abilities of two similarly sized congener ants as competitors for, and mutualists of pine‐feeding aphids, and how insectivorous birds affected each ant–aphid mutualism. Formica planipilis and F. podzolica were indistinguishable in forager abundance, but the former was 13‐fold more abundant at competition baits and provided 11‐fold more benefits to aphids. These results highlight how, in a single environment, a great ecological distance can exist between two congener ants of similar size. Insectivorous birds disrupted the two mutualisms to a similar extent, reducing aphid and ant abundance by 91% and 39% respectively. Nevertheless, birds had an important influence on the relative benefits of the two ants to aphids: where F. planipilis consistently benefited aphids, F. podzolica only did so in the absence of birds. Consequently, the presence of insectivorous birds and ant species identity jointly determined whether ant–aphid mutualisms occurred in pine canopies and the strength of such interactions. Our study highlights the inter‐relatedness of competition, predation and mutualism, and how competition can serve to strengthen mutualism by filtering inferior mutualists.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.     

Elevated temperatures alter an ant‐aphid mutualism

Ant‐hemipteran mutualisms are keystone interactions that can be variously affected by warming: these mutualisms can be strengthened or weakened, or the species can transition to new mutualist partners. We examined the effects of elevated temperatures on an ant‐aphid mutualism in the subalpine zone of the Rocky Mountains in Colorado, USA. In this system, inflorescences of the host plant, Ligusticum porteri Coult. & Rose (Apiaceae), are colonized by the ant‐tended aphid Aphis asclepiadis Fitch or less frequently by the non‐ant tended aphid Cavariella aegopodii (Scopoli) (both Hemiptera: Aphididae). Using an 8‐year observational study, we tested for two key mechanisms by which ant‐hemipteran mutualisms may be altered by climate change: shifts in species identity and phenological mismatch. Whereas the aphid species colonizing the host plant is not changing in response to year‐to‐year variation in temperature, we found evidence that a phenological mismatch between ants and aphids could occur. In warmer years, colonization of host plant inflorescences by ants is decreased, whereas for A. asclepiadis aphids, host plant colonization is mostly responsive to date of snowmelt. We also experimentally established A. asclepiadis colonies on replicate host plants at ambient and elevated temperatures. Ant abundance did not differ between aphid colonies at ambient vs. elevated temperatures, but ants were less likely to engage in tending behaviors on aphid colonies at elevated temperatures. Sugar composition of aphid honeydew was also altered by experimental warming. Despite reduced tending by ants, aphid colonies at elevated temperatures had fewer intraguild predators. Altogether, our results suggest that higher temperatures may disrupt this ant‐aphid mutualism through both phenological mismatch and by altering benefits exchanged in the interaction.     

Introduced ants reduce interaction diversity in a multi‐species,ant–aphid mutualism

Mutualisms contribute in fundamental ways to the origin, maintenance and organization of biological diversity. Introduced species commonly participate in mutualisms, but how this phenomenon affects patterns of interactions among native mutualists remains incompletely understood. Here we examine how networks of interactions among aphid‐tending ants, ant‐tended aphids, and aphid‐attacking parasitoid wasps differ between 12 spatially paired riparian study sites with and without the introduced Argentine ant Linepithema humile in southern California. To resolve challenges in species identification, we used DNA barcoding to identify aphids and screen for parasitoid wasps (developing inside their aphid hosts) from 170 aphid aggregations sampled on arroyo willow Salix lasiolepis. Compared to uninvaded sites, invaded sites supported significantly fewer species of aphid‐tending ants and ant‐tended aphids. At invaded sites, for example, we found only two species of ant‐tended aphids, which were exclusively tended by L. humile, whereas at uninvaded sites we found 20 unique ant–aphid interactions involving eight species of ant‐tended aphids and nine species of aphid‐tending ants. Ant–aphid linkage density was thus significantly lower at invaded sites compared to uninvaded sites. We detected aphid parasitoids in 14% (28/198) of all aphid aggregations. Although the level of parasitism did not differ between invaded and uninvaded sites, more species of wasps were detected within uninvaded sites compared to invaded sites. These results provide a striking example of how the assimilation of introduced species into multi‐species mutualisms can reduce interaction diversity with potential consequences for species persistence.     

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.     

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 effect size of aphid‐tending ants in an agricultural tri‐trophic system

Most studies regarding ant–aphid interactions focus only on the direct effects of ants on tended aphids and aphidophagous predators, or the indirect effects on the host plant. Studies evaluating the effects of aphid‐tending ants on more than one trophic level are rare and evaluate only the presence or absence of such effects. Here we assessed the effect sizes of ants in a tri‐trophic system (common bean plants, aphids and lacewing larvae). We tested if the presence of aphid‐tending ants has positive effects on aphid abundance and host‐plant production and negative effects on aphid predator abundance. We also hypothesized that aphid‐tending ants affect more intensely trophic levels that are more directly related to them (i.e., first aphids, then aphid predators and then host plants). We tested these hypotheses in field mesocosms experiments using the presence and absence of ants. We found that aphid‐tending ants have great positive effects on final aphid abundance. Ants also positively affected the number of seeds; however, it was not possible to measure the effect size for this trophic level. Furthermore, ants had negative effects on lacewing larvae only at first release. The effect size of ants was greater for aphids, followed by lacewing larvae, and with no effects on the number of seeds produced. Ants positively affect aphids and host‐plant production, probably by way of honeydew collection preventing the development of entomophagous/saprophytic fungi. On the other hand, ants negatively affect lacewing larvae by excluding them from the host plant. In natural systems, several ant species may attend aphids, differently affecting the organisms of the various trophic levels within the ant–aphid interaction, thereby obscuring the real effect size of ants. Assessing the effect size of aphid‐tending ants on the organisms involved in ant–aphid interactions provides more realistic information about the effects of this interaction on natural systems.     

Coexistence through mutualist‐dependent reversal of competitive hierarchies

Mechanisms that allow for the coexistence of two competing species that share a trophic level can be broadly divided into those that prevent competitive exclusion of one species within a local area, and those that allow for coexistence only at a regional level. While the presence of aphid‐tending ants can change the distribution of aphids among host plants, the role of mutualistic ants has not been fully explored to understand coexistence of multiple aphid species in a community. The tansy plant (Tanacetum vulgare) hosts three common and specialized aphid species, with only one being tended by ants. Often, these aphids species will not coexist on the same plant but will coexist across multiple plant hosts in a field. In this study, we aim to understand how interactions with mutualistic ants and predators affect the coexistence of multiple species of aphid herbivores on tansy. We show that the presence of ants drives community assembly at the level of individual plant, that is, the local community, by favoring one ant‐tended species, Metopeurum fuscoviride, while preying on the untended Macrosiphoniella tanacetaria and, to a lesser extent, Uroleucon tanaceti. Competitive hierarchies without ants were very different from those with ants. At the regional level, multiple tansy plants provide a habitat across which all aphid species can coexist at the larger spatial scale, while being competitively excluded at the local scale. In this case, ant mutualist‐dependent reversal of the competitive hierarchy can drive community dynamics in a plant–aphid system.     

Altitudinal variation in ant–aphid mutualism in nitrogen transfer of oak (<Emphasis Type="Italic">Quercus liaotungensis</Emphasis>)

Ant–plant relationship is a model for the study of the ecology and evolution of interspecific interactions. In direct ant–plant mutualism (i.e., plants providing food or nesting places for ants, and ants protecting the plants in return) ants provide nutrients to plants. However, whether a similar mechanism exists in indirect ant–plant mutualism (i.e., an ant–aphid–plant system) remains unknown. In this work, we used the ¹⁵N stable isotope method to study altitudinal variations in the roles of ants in the nutrient transfer of oak (Quercus liaotungensis). Our work shows that ants deliver nitrogen in indirect ant–plant interactions, and that the effect of nutrient transfer differed significantly with altitude. Ants’ trophic level at high altitudes was significantly lower than that at low altitudes, indicating that the degree of ant–aphid mutualism was greater at high altitudes, which may be beneficial in nitrogen transfer. Our work suggests that ant–aphid mutualism might be context dependent, such that it affects nutrient transfer in the food web, and that this context dependency is an important factor that influences altitudinal variation in nutrient transfer.     

The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms

Mutualisms are mutually beneficial interactions between species and are fundamentally important at all levels of biological organization. It is not clear, however, why one species participates in a particular mutualism whereas another does not. Here we show that pre-existing traits can dispose particular species to evolve a mutualistic interaction. Combining morphological, ecological, and behavioral data in a comparative analysis, we show that resource use in Chaitophorus aphids (Hemiptera: Aphididae) modulates the origin of their mutualism with ants. We demonstrate that aphid species that feed on deeper phloem elements have longer mouthparts, that this inhibits their ability to withdraw their mouthparts and escape predators and that, consequently, this increases their need for protection by mutualist ants.     

Ant attendance of the cotton aphid is beneficial for okra plants: deciphering multitrophic interactions

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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.     

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.     

Field experiments show contradictory short‐ and long‐term myrmecochorous plant impacts on seed‐dispersing ants

1. Some interactions previously described as mutualistic were revealed to be commensal or parasitic in subsequent investigations. Ant‐mediated seed dispersal has been described as a mutualism for more than a century; however, recent research suggests that it may be commensal or parasitic. Plants demonstrably benefit from ant‐mediated seed dispersal, although there is little evidence available to demonstrate that the interaction benefits long‐term ant fitness. 2. Field experiments were conducted in temperate North America focused on a key seed‐dispersing ant. All herbaceous plants were removed from a forest understorey for 13 years, and supplemented ant colonies with large elaiosome‐bearing seeds aiming to examine potential long‐ and short‐term myrmecochorous plant benefits for the ants. 3. If elaiosome‐bearing seeds benefit ants, suggesting a mutualistic relationship, it is expected that there would be greater worker and/or alate abundance and greater fat reserves (colony lipid content) with seed supplementation (short‐term) and in areas with high understorey herb abundance. 4. Short‐term seed supplementation of ant colonies did not result in an increase with respect to numbers or fat stores, although it did prompt the production of colony sexuals, which is a potential fitness benefit. In the long term, however, there was no positive effect on the ants and, instead, there were negative effects because the removal of elaiosome‐bearing plants corresponded with greater colony health. 5. The data obtained in the present study suggest that the ant–plant interaction ranged from occasionally beneficial to neutral to overall negative for the ant partner. Such results did not support considering the interaction as a mutualism. Collectively, the data suggest the need to reconsider the nature of the relationship between these ants and plants.     

Do exaptations facilitate mutualistic associations between invasive and native species?

As invasive species are key threats to ecosystem structure and function, it is essential to understand the factors underlying their success. Enigmatically, mutualistic organisms are often successful in colonizing novel environments even though they commonly persist only through intricate relationships with other species. Mutualistic ants, for example, protect aphids from natural enemies while collecting carbohydrate–rich honeydew. To facilitate this interaction, ants have evolved aggressive responses to aphid alarm pheromone emissions. As invasive and native mutualists have not evolved together, however, it is unclear if this form of cross-species communication exists between these two parties thereby facilitating these novel interactions. We address this hypothesis by assessing whether the invasive Argentine ant, Linepithema humile, responds to native poplar aphid, Chaitophorus populicola, alarm signals. Here, we show that interspecific signalling does exist in this newly established mutualistic interaction. Argentine ant workers exhibit increased aggression and double the number of visits to an aphid colony after an aphid alarm signal is emitted. We suggest that pre-adaptations may facilitate the emergence of mutualistic associations between many invasive and native species.     

Why do ants shift their foraging from extrafloral nectar to aphid honeydew?

When aphids parasitize plants with extrafloral nectaries (EFNs) and aphid colony size is small, ants frequently use EFNs but hardly tend aphids. However, as the aphid colony size increases, ants stop using EFNs and strengthen their associations with aphids. Although the shift in ant behavior is important for determining the dynamics of the ant–plant–aphid interaction, it is not known why this shift occurs. Here, we test two hypotheses to explain the mechanism responsible for this behavioral shift: (1) Extrafloral nectar secretion changes in response to aphid herbivory, or (2) plants do not change extrafloral nectar secretion, but the total reward to ants from aphids will exceed that from EFNs above a certain aphid colony size. To judge which mechanism is plausible, we investigated secretion patterns of extrafloral nectar produced by plants with and without aphids, compared the amount of sugar supplied by EFNs and aphids, and examined whether extrafloral nectar or honeydew was more attractive to ants. Our results show that there was no inducible extrafloral secretion in response to aphid herbivory, but the sugar concentration in extrafloral nectar was higher than in honeydew, and more ant workers were attracted to an artificial extrafloral nectar solution than to an artificial aphid honeydew solution. These results indicate that extrafloral nectar is a more attractive reward than aphid honeydew per unit volume. However, even an aphid colony containing only two individuals can supply a greater reward to ants than EFNs. This suggests that the ant behavioral shift may be explained by the second hypothesis.     

Sources of variation in the incidence of ant–aphid mutualism in boreal forests

• 1 The mutualism between wood ants of the Formica rufa group and aphids living in the canopy of trees is a widespread phenomenon in boreal forests, and it can affect tree growth. However, not all trees in the forest are involved in this interaction.
• 2 To assess the incidence of host trees involved in this ant–aphid mutualism and its spatial distribution in boreal forests, we inventoried sample plots with a radius of 10–15 m around wood ant mounds in 12 forest stands of two age classes (5–12‐year‐old sapling stands and 30–45‐year‐old pole stands) and two dominant tree species (Scots pine and silver birch) in Eastern Finland from 2007 to 2009.
• 3 The proportion of trees visited by ants out of all trees on the individual study plots were in the range 4–62%, and 1.5–39% of the trees on the plots were consistently visited by ants during all 3 years. The percentage of host trees increased with the ant mound base area on the plots. Trees visited by ants were larger and closer to the mound than trees not visited by ants. Within the group of visited trees, more ants were found on bigger trees and on trees close to the ant mounds.
• 4 Extrapolated from plot to stand level, we estimated that 0.5–6.6% of the trees were host trees in at least one of the three study years, and that only 0.01–2.3% of all the trees were consistently visited by ants during all 3 years. It is concluded that ant–aphid mutualism is a minor occurrence at the stand level.

     

Ants indirectly reduce the reproductive performance of a leafless shrub by benefiting aphids through predator deterrence

Ant–aphid mutualisms can generate cascade effects on the host plants, but these impacts depend on the ecological context. We studied the consequences of ant–aphid interactions on the reproductive performance of a Mediterranean leafless shrub (Retama sphaerocarpa), through direct and indirect effects on the arthropod community. By manipulating the presence of ants and aphids in the field, we found that ants increased aphid abundance and their persistence on the plant and reduced aphid predators by nearly half. However, the presence of ants did not affect the abundance of other plant herbivores, which were relatively scarce in the studied plants. Aphids, and particularly those tended by ants, had a negative impact on the plant reproductive performance by significantly reducing the number of fruits produced. However, fruit and seed traits were not changed by the presence of aphids or those tended by ants. We show that ants favoured aphids by protecting them from their natural enemies but did not indirectly benefit plants through herbivory suppression, resulting in a net negative impact on the plant reproductive performance. Our study suggests that the benefits obtained by plants from hosting ant–aphid mutualisms are dependent on the arthropod community and plant traits.