Ant-aphid Mutualism Research Articles

Anti-mite measures of aphids for protecting ants promote persistence of ant-aphid mutualism

Anti-mite measures of aphids for protecting ants promote persistence of ant-aphid mutualism

Host plant phenology shapes aphid abundance and interactions with ants

Phenological mismatch can occur when plants and herbivores differentially respond to changing phenological cues, such as temperature or snow melt date. This often shifts herbivore feeding to plant stages of lower quality. How herbivores respond to plant quality may be also mediated by temperature, which could lead to temperature‐by‐phenology interactions. We examined how aphid abundance and mutualism with ants were impacted by temperature and host plant phenology. In this study system, aphids Aphis asclepiadis colonize flowering stalks of the host plant, Ligusticum porteri. Like other aphids, abundance of this species is dependent on ant protection. To understand how host plant phenology and temperature affect aphid abundance, we used a multiyear observational study and a field experiment. We observed 20 host plant populations over five years (2017–2021), tracking temperature and snow melt date as well as host plant phenology and insect abundance. We found host plant and aphid phenology to differentially respond to temperature and snow melt timing. Early snow melt accelerated host plant phenology to a greater extent than aphid phenology, which was more responsive to temperature. Both the likelihood of aphid colony establishment and ant recruitment were reduced when aphids colonized host plants at post‐flowering stages. In 2019, we experimentally accelerated host plant phenology by advancing snow melt date by two weeks. We factorially combined this treatment with open top warming chambers surrounding aphid colonies. Greatest growth occurred for colonies under ambient temperatures when they occurred on host plants at the flowering stage. Altogether, our results suggest that phenological mismatch with host plants can decrease aphid abundance, and this effect is exacerbated by temperature increases and changes to the ant–aphid mutualism.

Providing sugar sources for ants improves the biological control of Aphis spp. in apple orchards

The green apple aphids Aphis pomi DeGeer and A. spiraecola Patch are serious pests of apple, especially in young orchards, where both species establish facultative mutualisms with ants. This study, conducted in Hungary in 2014 and 2015, manipulated the presence of the common black ant Lasius niger (L.) on colonies of Aphis spp. in apple tree canopies. To this end, two kinds of sugar dispensers (bottle dispensers and agar jelly cubes), each providing a sucrose solution with 300 g/1000 ml concentration, were deployed as alternative sugar sources for the ants, with plots lacking dispensers serving as controls. Both forms of sugar provisioning reduced the number of ants tending Aphis spp. colonies and reduced aphid populations compared to controls in both years. However, bottle dispensers demonstrated consistent efficacy in both years, whereas agar jelly cubes were less reliable in distracting the ants. Both treatments significantly increased the abundance of natural enemies at Aphis spp. colonies compared to controls. Our results indicate that the provisioning of ants with sugar in apple orchards can effectively disrupt ant-aphid mutualisms in the case of Aphis spp., by drawing ants away from aphid colonies and thus increasing natural enemy predation on aphid colonies. The use of sugar-feeding tactics to alter ant behaviour should permit reduced pesticide use in apple orchards, whether to control aphids or other pests that might serve as prey for ants, and is fundamentally compatible with biological pest control in apple orchards.

Evolution: Ant trail pheromones promote ant–aphid mutualisms

A new study shows that trail pheromones produced by an invasive ant species suppress the dispersal and stimulate the reproduction of cotton aphids that the ants can 'milk' for honeydew. Aphids use these pheromones as a signal of ant presence and respond adaptively, analogous to early stages of animal husbandry where animals were attracted to human settlements.

Wood ants prefer conifers to broadleaved trees in mixed temperate forests

Abstract Wood ants, species of the subgenus Formica s. str., are one of the most important groups of insects in forest ecosystems due to their high abundance and activity. We assessed the foraging pressure of Formica polyctena and Formica rufa, two dominant wood ant species in the Białowieża Forest. In addition, we compared coniferous and mixed stands in these respects. In mixed stands F. polyctena visited more trees per plot than F. rufa. F. polyctena might forage a larger area due to higher population sizes, which further confirms higher foraging pressure of F. polyctena in comparison with F. rufa. In our study area, host trees of the ant–aphid mutualism were larger in diameter than nonhost trees. The ants also preferred trees situated closer to their nests. In both mixed and coniferous stands, the most visited tree species was Norway spruce. Thus, we can conclude that Norway spruce seems to be preferred by the ant. The decline of living spruce in the Białowieża Forest may endanger their food source and impact the vitality of ant colonies.

Ant-induced evolutionary patterns in aphids.

This review investigates ant-aphid mutualism (trophobiosis), in particular focusing on evolutionary processes in aphids resulting from this interaction. This broad literature review allows us to revise existing views on certain aspects of this mutualism and provide the first timeline of its possible development over a geological timescale. We propose a new classification of ant-aphid mutualism with respect to its ecological characteristics and present new explanations of the development of certain morphological structures of aphids as resulting from adaptation to a trophobiotic relationship with ants. In light of these findings, the presence of the so-called 'trophobiotic organ' in all myrmecophilous aphids is questioned. We review various communication modes between aphids and mutualistic ants and the possible influence of this symbiosis on modifications of aphid life cycles. Recent evidence on the suspected role of endosymbiotic bacteria in the development of mutualism is discussed. Finally, we propose a first timeline of ant-aphid interactions leading to the development of particular adaptations of aphids to mutualism, from general interactions between diverging Aphidomorpha and ants in the late Mesozoic to more specific coevolution between the aphid tribe Fordini and the ant genus Lasius.

Seasonal Changes in Sugar and Amino Acid Preference in Red Wood Ants of The Formica rufa Group

Red wood ants of the Formica rufa group are important ecosystem engineers throughout the Northern Hemisphere with potential to be commercially produced and used as predatory agents in biological control programs. However, in order to do that, their mutualistic relationship with aphids needs to be disrupted. This may be achieved by developing artificial sugar-based solutions with a composition that makes them more attractive than aphid honeydew. The present field study investigated Formica rufa’s preference for several sugar and amino acid sources, as well as potential seasonal changes in these preferences. Red wood ants consistently preferred sucrose to monosaccharides and were most attracted to solutions containing an amino acid source, albeit seasonal differences were observed with regard to which amino acid sources were most preferred. Recruitment to offered sugar solutions was highest during July, when colony requirements were high, and during October, when alternative food sources were scarce. Since ant preference for sugar solution constituents seems to be species-specific and show seasonal dynamics, artificial food aimed at disrupting ant-aphid mutualisms should be tailored to individual species and seasons.

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.

Progressive sensitivity of trophic levels to warming underlies an elevational gradient in ant–aphid mutualism strength

Although species interactions are often proposed to be stronger at lower latitudes and elevations, few studies have evaluated the mechanisms driving such patterns. In this study, we assessed whether, and by which mechanisms, abiotic changes associated with elevation altered the outcome of an ant–aphid protection mutualism. To do so, we characterized the multi‐trophic interactions among the ant Formica podzolica, the aphid Aphis varians, and aphid natural enemies occurring on the plant Chamerion angustifolium within replicate high and low elevation valleys. Low (versus high) elevation sites had longer summers (snowmelt 13 days earlier) and were on average 1.1°C warmer and 41% drier throughout the year. At low elevations, individual ant colonies consumed approximately double the volume of carbohydrate baits, likely due to a higher foraging tempo, and possibly due to a greater demand for sugar‐ versus protein‐rich resources (as indicated by stable isotope analysis). Wild aphid colonies at low elevations were visited by 1.4‐fold more natural enemies (controlling for variation in aphid abundance), while experimental aphid colonies on potted plants were tended 52% more frequently by ants. As a result, ants increased aphid colony survival by 66% at low elevations but had no detectable effect at high elevations; at low (versus high) elevations aphid colonies without ants had lower survival, demonstrating stronger predator effects, while aphid colonies with ants had higher survival, demonstrating even stronger ant benefits. Analyses for the effects of mean summer temperature yielded qualitatively identical results to those based on elevation. Collectively, these findings support predictions for a greater sensitivity of higher trophic levels to warming and demonstrate how species interactions can vary across environmental gradients due to simultaneous changes in species traits and abundances across multiple trophic levels.

Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids.

Animal mutualisms, which involve beneficial interactions between individuals of different species, are common in nature. Insect-insect mutualism, for example, is widely regarded as a keystone ecological interaction. Some mutualisms are anticipated to be modified by climate change, but the focus has largely been on plant-microbe and plant-animal mutualisms rather than those between animals. Ant-aphid mutualisms, whereby ants tend aphids to harvest their honeydew excretions and, in return, provide protection for the aphids, are widespread. The mutualism is heavily influenced by the quality and quantity of honeydew produced by aphids, which is directly affected by host plant quality. As predicted increases in concentrations of atmospheric carbon dioxide (eCO2 ) are widely reported to affect plant nutritional chemistry, this may also alter honeydew quality and hence the nature of ant-aphid mutualisms. Using glasshouse chambers and field-based open-top chambers, we determined the effect of eCO2 on the growth and nutritional quality (foliar amino acids) of lucerne (Medicago sativa). We determined how cowpea aphid (Aphis craccivora) populations and honeydew production were impacted when feeding on such plants and how this affected the tending behaviour of ants (Iridomyrmex sp.). eCO2 stimulated plant growth but decreased concentrations of foliar amino acids by 29% and 14% on aphid-infested plants and aphid-free plants, respectively. Despite the deterioration in host plant quality under eCO2 , aphids maintained performance and populations were unchanged by eCO2 . Aphids induced higher concentrations of amino acids (glutamine, asparagine, glutamic acid and aspartic acid) important for endosymbiont-mediated synthesis of essential amino acids. Aphids feeding under eCO2 also produced over three times more honeydew than aphids feeding under ambient CO2 , suggesting they were imbibing more phloem sap at eCO2 . The frequency of ant tending of aphids more than doubled in response to eCO2 . To our knowledge, this is the first study to demonstrate the effects of atmospheric change on an ant-aphid mutualism. In particular, these results highlight how impending changes to concentrations of atmospheric CO2 may alter mutualistic behaviour between animals. These could include positive impacts, as reported here, shifts from mutualism to antagonism, partner switches and mutualism abandonment.

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.

Does urbanization explain differences in interactions between an insect herbivore and its natural enemies and mutualists?

Urbanization can alter the composition of arthropod communities. However, little is known about how urbanization affects ecological interactions. Using experimental colonies of the black bean aphid Aphis fabae Scopoli reared on Vicia faba L, we asked if patterns of predator-prey, host-parasitoid and ant-aphid mutualisms varied along an urbanization gradient across a large town in southern England. We recorded the presence of naturally occurring predators, parasitoid wasps and mutualistic ants together with aphid abundance. We examined how biotic (green areas and plant richness) and abiotic features (impervious surfaces and distance to town center) affected (1) aphid colony size, (2) the likelihood of finding predators, mutualistic ants and aphid mummies (indicating the presence of parasitoids), and (3) how the interplay among these factors affected patterns of parasitoid attack, predator abundance, mutualistic interactions and aphid abundance. Aphid abundance was best explained by the number of mutualistic ants attending the colonies. Aphid predators responded negatively to both the proportion of impervious surfaces and to the number of mutualistic ants farming the colonies, and positively to aphid population size, whereas parasitized aphids were found in colonies with higher numbers of aphids and ants. The number of mutualistic ants attending was positively associated with aphid colony size and negatively with the number of aphid predators. Our findings suggest that for insect-natural enemy interactions, urbanization may affect some groups, while not influencing others, and that local effects (mutualists, host plant presence) will also be key determinants of how urban ecological communities are formed.

Multitrophic interactions mediate the effects of climate change on herbivore abundance.

Climate change can influence the abundance of insect herbivores through direct and indirect mechanisms. In this study, we evaluated multitrophic drivers of herbivore abundance for an aphid species (Aphis helianthi) in a subalpine food web consisting of a host plant (Ligusticum porteri), mutualist ants and predatory lygus bugs (Lygus spp.). We used a model-selection approach to determine which climate and host plant cues best predict year-to-year variation in insect phenology and abundance observed over 6years. We complemented this observational study with experiments that determined how elevated temperature interacts with (1) host plant phenology and (2) the ant-aphid mutualism to determine aphid abundance. We found date of snowmelt to be the best predictor of yearly abundance of aphid and lygus bug abundance but the direction of this effect differed. Aphids achieved lower abundances in early snowmelt years likely due to increased abundance of lygus bug predators in these years. Elevating temperature of L. porteri flowering stalks reduced their quality as hosts for aphid populations. However, warming aphid colonies on host plants of similar quality increased population growth rates. Importantly, this effect was apparent even in the absence of ants. While we observed fewer ants tending colonies at elevated temperatures, these colonies also had reduced numbers of lygus bug predators. This suggests that mutualism with ants becomes less significant as temperature increases, which contrasts other ant-hemipteran systems. Our observational and experimental results show the importance of multitrophic species interactions for predicting the effect of climate change on the abundances of herbivores.

Altitudinal variation in ant–aphid mutualism in nitrogen transfer of oak (Quercus liaotungensis)

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.

Effect of ant attendance on aphid population growth and above ground biomass of the aphid's host plant

Ant-aphid mutualism is considered to be a beneficial association for the individuals concerned. The population and fitness of aphids affected by ant attendance and the outcome of this relationship affects the host plant of the aphid. The main hypothesis of the current study is that ant tending decreases aphid developmental time and/or increases reproduction per capita, which seriously reduces host plant fitness. The effect of attendance by the ant Tapinoma erraticum (Latreille, 1798) (Hymenoptera: Formicidae) on population growth and duration of different developmental stages of Aphis gossypii Glover (Hemiptera: Aphididae) were determined along with the consequences for the fitness of the host plant of the aphid, Vicia faba L., in greenhouse conditions. The initial aphid density was manipulated in order to study aphid performance due to density-dependent changes in ant attendance. The population growth rate of ant attended aphids was more than that of unattended aphids. However, the ratio of 1st-2nd nymphs to adults in aphid populations attended by ants was lower. The yields of bean plants on which the aphids were attended by ants were significantly greater than those of unattended plants. This study indicates that ants not only increase aphid fitness in terms of their population growth rate, but also benefit the host plant.

アリ-アブラムシ共生系における今後の展望 : 内部共生細菌や天敵群集を含めた複合共生系とアブラムシの適応との相互作用

アリ-アブラムシ共生系における今後の展望 : 内部共生細菌や天敵群集を含めた複合共生系とアブラムシの適応との相互作用

The effect of host plants on genotype variability in fitness and honeydew composition of Aphis fabae.

Aphid species can be polyphagous, feeding on multiple host plants across genera. As host plant species can have large variation in their phloem composition, this can affect aphid fitness and honeydew composition. Previous research showed significant intraspecific genotype variation in the composition of the honeydew carbohydrates of the black bean aphid Aphis fabae, with the ant attractant trisaccharide melezitose showing especially large variation across different genotypes. In this study, we test if variation in melezitose and carbohydrate composition of aphid honeydew could be linked to the adaptation of specific aphid genotypes to particular host plants. To this end, 4 high and 5 low melezitose secreting genotypes of the black bean aphid Aphis fabae were reared on 4 common host plants: broad bean, goosefoot, beet, and poppy. The carbohydrate composition, and in particular melezitose secretion, showed important aphid genotype and host plant interactions, with some genotypes being high melezitose secreting on 1 host plant but not on another. However, the interaction effects were not paralleled in the fitness measurements, even though there were significant differences in the average fitness across the different host plants. On the whole, this study demonstrates that aphid honeydew composition is influenced by complex herbivore-plant interactions. We discuss the relevance of these findings in the context of ant-aphid mutualisms and adaptive specialization in aphids.

Aphid–Buchnera–Ant symbiosis; or why are aphids rare in the tropics and very rare further south?

ABSTRACTAt least since the Cretaceous Terrestrial Revolution, the geographical distribution of aphids, particularly in the Northern Hemisphere, has been strongly affected by the low thermal tolerance of their obligatory bacterial symbiont,Buchnera aphidicola, which was why the aphids switched to obligate parthenogenesis in low latitudes. Hormaphidids and greenideids penetrated into the tropics only after the Oligocene strengthening of climate seasonality, and specialisations of the tropical representatives of these families did not allow them to spread further south (in the case of cerataphidines), or only allowed in few cases (in the case of greenideids).Aphids suffered from the Mesozoic–Cenozoic boundary extinction event much more strongly than other insects. The extinction was roughly coincidental with the establishment of the tight symbiosis of aphids with formicine and dolichoderine ants, which was accompanied by the flourishing of all three groups.In the Cretaceous, all of the representatives of extant and subfamilies occupied positions that were subordinate to Armaniinae and Sphecomyrminae. Prior to large ant colonies evolving their efficient ant–aphid mutualism, the aphids remained unprotected before the growing ant predation. The origin of the aphid trophobiosis with large colonies of Formicinae and Dolichoderinae has resulted in the steep decline of aphids left beyond that ant–aphid symbiotic network. By at least the basal Eocene (unlike the Late Cretaceous), ant proportions in the entomofauna increased sharply, and evident dominants emerged. Even now, aphid milkers from small colonies (hundreds of specimens) never protect their symbionts, and homopteran-tending ants are more likely to be dominant, with large colonies of 104–105workers.The mutualistic ant–aphid system failed to cross the tropical belt during the Cenozoic because ofBuchnera's low heat tolerance. As a result, the native southern temperate aphid fauna consists now of seven genera only, five of which are Late Cretaceous relicts. Some of them had relatives in Late Cretaceous amber of the Northern Hemisphere.

Can artificial nectaries outcompete aphids in ant-aphid mutualism? Applying artificial sugar sources for ants to support better biological control of rosy apple aphid, Dysaphis plantaginea Passerini in apple orchards

The rosy apple aphid, Dysaphis plantaginea Passerini, is a serious pest in apple orchards. It establishes close facultative mutualistic relationships with ants. An experiment manipulating the presence of the common black ant, Lasius niger (L.), in colonies of D. plantaginea in the canopy of apple trees by provision of ant-feeders (artificial nectaries) containing sucrose solution as an alternative sugar source were conducted in apple orchards in the United Kingdom and Hungary to test if this method can regulate densities of D. plantaginea below the threshold for economic damage through enhancing the activity of its natural enemies. Apple trees with physical ant-exclusion (sticky barriers) and without any treatment were used as controls.Ant-feeding with sucrose solution, in a similar way to physical ant exclusion, effectively reduced the numbers of ants tending D. plantaginea colonies and it consequently resulted in a reduction in D. plantaginea populations in both studies. In spite of marked differences in natural enemy abundance and composition found in UK and Hungary, both treatments caused significant increases in natural enemy (e.g. Dermaptera, Heteroptera, Coccinellidae, Syrphidae) pressure on D. plantaginea. Our results show that supplementary sugar feeding of ants is a successful method for supporting biocontrol of rosy apple aphid through enhancing the effectiveness of its natural enemies. This new biocontrol approach to control aphids in apple orchards is likely to substantially reduce the need for aphicide sprays in orchards and is compatible with organic pest control. The implications of these results for supporting better biological control of aphids in apple orchards are discussed.

Mixed effects of ant–aphid mutualism on plants across different spatial scales

Scale affects how we observe, explain, and predict patterns and processes in ecology. The pattern of biotic interactions can be scale-dependent, but it is not clear how biotic interactions perform at different scales. We tested the effects of aphid-tending ants Lasius fuliginosus on the oak tree Quercus liaotungensis by excluding ants at two scales (branches and whole trees). Furthermore, we explored the variation of the effects on different-size branches and trees. The ants had significant anti-herbivory effects, a positive effect on aphids, but a negative effect on galls. Contrary to previous assumptions, effects of ants on plants and herbivores are similar between the branch and plant scales. The size of the branch or tree also had no impact on the ecological effects of ants, indicating the ecological effect of ant–aphid mutualism is consistent within and among individual trees. The homogeneous distribution of aphids may be the key reason for the scale-independent effect of the indirect ant–plant interaction. Our finding highlights the importance of biotic defense for plants across different spatial scales.