Influence of macronutrient imbalance on native ant foraging and interspecific interactions in the field

1. Ants interact with a diversity of organisms. These interactions, coupled with their abundance, cause ants to have ecologically important effects across multiple trophic levels. 2. Empirical study of ant nutritional ecology has led to the prediction that a macronutrient imbalance will affect ant behaviour and interspecific interactions that underlie these broad‐scale effects. Excess carbohydrate relative to protein is predicted to increase ant aggressiveness, predatory tendency and foraging activity, and to decrease collection of hemipteran honeydew and plant nectar. 3. In field experiments conducted in 2009 and 2010, captive colony fragments of a native ant, Formica podzolica (Hymenoptera: Formicidae), were provided with either simulated prey or carbohydrate solution ad libitum. Foraging behaviours and interactions with flowers, myrmecophilous aphids and aphid natural enemies on wild‐grown plants were documented. 4. Strong effects of macronutrient imbalance on foraging manifested quickly and consistently across colonies; in accordance with predictions, prey‐fed foragers collected both honeydew and floral nectar, whereas carbohydrate‐fed ants ceased collecting these resources. Counter to predictions, carbohydrate‐fed ants dramatically lowered their activity levels and did not prey upon aphids. 5. Ants had no effect on aphid enemies in 2009, when the latter were relatively rare, but decreased their abundance in 2010. Despite this protection, the net effect of ants on aphids was negative (measured only in 2009). Prey‐fed ants demonstrated a strong preference for honeydew over floral nectar, thus demonstrating that a macronutrient imbalance may lead to different interactions with similar resources. 6. This study links ant nutrition and community ecology by demonstrating the rapid, asymmetric and multitrophic consequences of nutritionally mediated behaviour.     

Effects of prey aphid species on the abundance of a parasitoid and two predator species in aphid colonies attended by ants on citrus

This study focused on three species of enemies, the parasitoid wasp Lysiphlebus japonicus Ashmead (Hymenoptera: Aphidiidae), the ladybird Scymnus posticalis Sicard (Coleoptera: Coccinellidae) and the predatory gall midge Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), all of which are able to exploit aphids attended by ants. I experimentally evaluated the effects of prey aphid species on the abundance of each of the three enemy species in ant‐attended aphid colonies on citrus. The aphids compared were Aphis gossypii Glover versus Aphis spiraecola Patch in late spring, and Toxoptera citricidus (Kirkaldy) versus A. spiraecola in late summer (all, Hemiptera: Aphididae). Colonies of the three aphid species were attended by the ant Pristomyrmex punctatus Smith (Hymenoptera: Formicidae). The initial number of attending ants per individual aphid did not differ significantly between the colonies of the two aphid species compared in each season. Between A. gossypii and A. spiraecola, there was no significant difference in the number of mummies formed by the parasitoid or foraging larvae of each of the two predators per aphid colony. A significant difference was detected between T. citricidus and A. spiraecola for each of the three enemy species, with a far greater number of L. japonicus mummies in T. citricidus colonies and distinctly more larvae of each of the two predators in A. spiraecola colonies. Thus, the abundance of each of the three enemy species in ant‐attended aphid colonies was significantly influenced by the species of the prey aphids, with the three enemies showing different responses to the three aphid species.     

Differential host use in two highly specialized ant-plant associations: evidence from stable isotopes

Carbon and nitrogen stable isotopes were used to examine variation in ant use of plant resources in the Cecropia obtusifolia / Azteca spp. association in Costa Rica. Tissue of ants, host plants and symbiotic pseudococcids were collected along three elevation transects on the Pacific slope of Costa Ricas Cordillera Central, and were analyzed for carbon and nitrogen isotopic composition. Worker carbon and nitrogen signatures were found to vary with elevation and ant colony size, and between Azteca species groups. Ants in the A. constructor species group appear to be opportunistic foragers at low elevations, but rely more heavily on their host plants at high elevations, whereas ants in the A. alfari species group consume a more consistent diet across their distribution. Further, isotope values indicate that both ant species groups acquire more nitrogen from higher trophic levels at low elevation and when ant colonies are small. Provisioning by the host is a substantial ecological cost to the interaction, and it may vary, even in a highly specialized association. Nonetheless, not all specialized interactions are equivalent; where interaction with one ant species group appears conditional upon the environment, the other is not. Differential host use within the Cecropia-Azteca association suggests that the ecological and evolutionary benefits and costs of association may vary among species pairs.     

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.     

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.     

Effect of Invasive Species of Herbaceous Plants and Associated Aphids (Hemiptera,Sternorrhyncha: Aphididae) on the Structure of Ant Assemblages (Hymenoptera,Formicidae)

—In 2015–2017, attendance of 15 invasive and 22 native species of herbaceous plants by ants was studied in 6 habitats in the environs of Kyiv (Ukraine). Altogether, 14 ant species were found, of which 12 were recorded on invasive plants and 9 on native plants; 8 aphid species were found on 8 invasive plant species. Five invasive plant species (Asclepias syriaca, Heracleum mantegazzianum, Oenothera biennis, Onopordum acanthium, and Amaranthus retroflexus) were found to be attractive to ants, with over a half of all the ant workers in all the habitats being recorded on them; besides, numerous colonies of 7 aphid species were also found on these plants. These invasive plants positively affect the structure of ant assemblages since the aphid colonies provide ants with food resource. The remaining 10 invasive plant species, including 5 transformer species, were poorly visited by ants and housed no aphid colonies, with the exception of Conyza canadensis on which the non-myrmecophilous aphid Uroleucon erigeronense (Thomas, 1878) was found. Two thirds of invasive plant species had a negative effect on the structure of ant assemblages because they replaced the native plants and thus reduced the trophic resources of aphids.

     

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.     

Behavioral mechanisms underlying ants' density-dependent deterrence of aphid-eating predators

Density-dependent mutualisms have been well documented, but the behavioral mechanisms that can produce such interactions are not as well understood. We investigated interactions between predatory ladybirds and the ant Lasius neoniger, which engages in a facultative association with the aphid Aphis fabae . We found that ants disrupted predator aggregation and deterred foraging, but that this effect varied with aphid density. In the field, smaller aphid colonies had higher numbers of ants per aphid (higher relative ant density), whereas plants with larger aphid colonies had lower relative ant density. Ants deterred ladybird foraging when relative ant density was high, but when relative ant density was low, ladybirds aggregated to aphids and foraged more successfully. This difference in ladybird foraging success appeared to be driven by variation in the ants' distribution on the plant and the ladybirds' reaction to ants. When relative ant density was high, ants moved around the perimeter of the aphid colonies, which resulted in faster detection of predators and a greater likelihood of ladybirds leaving. However, when relative ant density was low, ants moved only in the midst of the aphid colonies and rarely around the perimeter, which allowed predators to approach the aphid colony from the perimeter and feed without detection. Such predators were less likely to leave the aphid colony when subsequently detected by ants. We suggest that differences in relative ant numbers, ant distribution, and predator reaction to detection by ants could lead to complex population-level consequences including density-dependent mutualisms and the possibility that predators act as prudent predators.     

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.     

Changes in Species Richness,Abundance, and Composition of Arboreal Twig‐nesting Ants Along an Elevational Gradient in Coffee Landscapes

The distribution, diversity, and assembly of tropical insects have long intrigued ecologists, and for tropical ants, can be affected by competitive interactions, microhabitat requirements, dispersal, and availability and diversity of nesting sites. Arboreal twig‐nesting ants are limited by the number of hollow twigs available, especially in intensive agricultural systems. Ant diversity and abundance may shift along elevation gradients, but no studies have examined if the proportion of occupied twigs or richness of arboreal twig‐nesting ants vary with elevation. In coffee agroecosystems, there are over 40 species of arboreal twig‐nesting ants. We examined communities of twig‐nesting ants in coffee plants along an elevational gradient to answer the following questions: (1) Do species richness and colony abundance decline with elevation or show a mid‐elevation peak? (2) Does community composition change with elevation? (3) Is elevation an important predictor of change in ant abundance, richness, and relative abundance of common species? We surveyed 42 10 × 10 m plots in 2013 from 450 to1550 m elevation across a coffee landscape in Chiapas, Mexico. We sampled a total of 2211 hollow coffee twigs, 77.1 percent of which were occupied by one of 28 species of ants. Pseudomyrmex simplex was more abundant in lower elevations, whereas Pseudomyrmex ejectus dominated in high elevations. Species richness and the percent of occupied hollow twigs both peaked at mid‐elevations (800–1050 m). In sum, we found that species richness, abundance, and composition of arboreal twig‐nesting ants shift with elevation. These findings may provide important insights for understanding ant communities in coffee agroecosystems.     

Bottom-up effects may not reach the top: the influence of ant-aphid interactions on the spread of soil disturbances through trophic chains

Soil disturbances that increase nutrient availability may trigger bottom-up cascading effects along trophic chains. However, the strength and sign of these effects may depend on attributes of the interacting species. Here, we studied the effects of nutrient-rich refuse dumps of the leaf-cutting ant, Acromyrmex lobicornis, on the food chain composed of thistles, aphids, tending ants and aphid natural enemies. Using stable isotopes tracers, we show that the nitrogen accumulated in refuse dumps propagates upward through the studied food chain. Thistles growing on refuse dumps had greater biomass and higher aphid density than those growing in adjacent soil. These modifications did not affect the structure of the tending ant assemblage, but were associated with increased ant activity. In contrast to the expectations under the typical bottom-up cascade effect, the increase in aphid abundance did not positively impact on aphid natural enemies. This pattern may be explained by both an increased activity of tending ants, which defend aphids against their natural enemies, and the low capacity of aphid natural enemies to show numerical or functional responses to increased aphid density. Our results illustrate how biotic interactions and the response capacity of top predators could disrupt bottom-up cascades triggered by disturbances that increase resource availability.     

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

相似文献   

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.     

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.     

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.     

Landscape complexity differentially benefits generalized fourth,over specialized third,trophic level natural enemies

The differential loss of higher trophic levels in the face of natural habitat loss can result in the disruption of important trophic interactions, such as biological control. Natural enemies of herbivorous pests in cropping systems often benefit from the presence of natural habitats in surrounding landscapes, as they provide key resources such as alternative hosts. However, any benefits from a biological control perspective may be dampened if this also enhances enemies at the fourth trophic level. Remarkably, studies of the influence of landscape structure on diversity and interactions of fourth trophic‐level natural enemies are largely lacking. We carried out a large‐scale sampling study to investigate the effects of landscape complexity (i.e. the proportion of non‐crop habitat in the landscapes surrounding focal study areas) on the parasitoid communities of aphids in wheat and on an abundant extra‐field plant, stinging nettle. Primary parasitoid communities (3rd trophic level) attacking the cereal aphid, Sitobion avenae, had little overlap with the communities attacking the nettle aphid, Microlophium carnosum, while secondary parasitoids (4th trophic level) showed high levels of species overlap across these two aphids (25 vs 73% shared species respectively), resulting in significantly higher linkage density and lower specialization for secondary than primary parasitoid webs. In wheat, parasitoid diversity was not related to landscape complexity for either primary or secondary parasitoids. Rates of primary parasitism were generally low, while secondary parasitism rates were high (37–94%) and increased significantly with increasing landscape complexity, although this pattern was driven by a single secondary parasitoid species. Overall, our results demonstrate that extra‐field habitats and landscape complexity can differentially benefit fourth, over third, trophic level natural enemies, and thereby, could dampen biological control. Our results further suggest that fourth trophic‐level enemies may play an important, yet understudied, role in linking insect population dynamics across habitat types.     

Evidence for the transfer of a soil‐borne contaminant from plants to ants via an aphid mediator

1. Uptake of environmental contaminants by lower trophic groups can have negative effects on higher trophic groups. This study tested the ability of selenium, an environmental contaminant found in high concentrations throughout the tissues of certain accumulating plants, to be transferred to ants via aphid tissue and honeydew. 2. Plants of the selenium accumulator, Raphanus sativus (wild radish), were watered with three different selenium treatments (0, 0.25 or 0.5 µg Se ml^?1). Aphids, Myzus persicae, and Argentine ant colonies, Linepithema humile, were added to each caged plant and allowed to interact freely. Ant colonies were supplemented with one of three different food options to encourage the consumption of aphids, aphid honeydew, or aphids and honeydew. 3. The accumulation of selenium by each trophic group and a trophic transfer factor (TTF) was calculated. The TTF for plants to aphids was > 1, indicating biomagnification, whereas the TTF for aphids to worker ants was < 1, indicating only biotransfer. Accumulated levels by worker ants did not statistically differ as a result of diet. 4. The amounts of selenium acquired by ants as a factor of diet and caste were compared. Plants, aphids and worker ants accumulated selenium in a dose‐dependent manner. Ant queens did not contain detectable amounts of selenium. Honeydew contained comparable amounts of selenium to plant selenium levels. 5. Access to toxic compounds via honeydew and insect protein may have negative effects on the range expansion of invasive species, such as the Argentine ant.     

Quarantining behaviour of ants towards infected aphids as an antifungal mechanism in ant–aphid interactions

The ecological success of social insects, including ants, is tightly connected with their ability to protect themselves and their food resources. In exchange for energy‐rich honeydew, ants protect myrmecophilous aphids from various natural enemies. Fungal infection can have disastrous consequences for both mutualist partners, wherein aphids can be disease vectors. Behavioural responses towards fungus‐infected aphids of ant species in nature have scarcely been studied. Here, we studied the behaviour of honeydew foragers of four ant species – Formica polyctena Foerster, Formica rufa L., Formica pratensis Retzius (Hymenoptera: Formicidae, Formicini), and Lasius niger (L.) (Formicidae, Lasiini) – towards Symydobius oblongus (von Heyden) aphids contaminated with the generalist fungal pathogen Beauveria bassiana (Balsamo‐Crivelli) Vuillemin in the field. Aphid milkers from Formica spp. quickly detected and removed infected aphids from the host plant (Betula pendula Roth., Betulaceae). Neither ant species, the degree of aphid‐milker specialization (medium or high), nor the number of honeydew foragers had significant effects on the behaviour of Formica milkers towards infected aphids. Unlike Formica ants, L. niger usually displayed non‐aggressive behaviour (tolerance, antennation, honeydew collection, grooming). By the immediate removal of infected insects, Formica ants seem to minimize the probability of infection of symbionts as well as themselves. Quarantining behaviour may play an important role in ant–aphid interactions as a preventive antifungal mechanism formed under parasite pressure and thus contributing to the ecological success of ants.     

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.     

Context‐dependence in an ant–aphid mutualism: direct effects of tending intensity on aphid performance

1. In ant–hemipteran mutualisms, ants receive carbohydrates in the form of honeydew, while hemipterans receive protection from natural enemies. In the absence of natural enemies, however, the direct effects of tending are generally less well known. We hypothesised that with increasing tending intensity (ant to aphid ratio), aphid performance would increase initially, then decrease at high tending levels due to the metabolic cost of producing high quality honeydew. 2. We tested our hypothesis in a greenhouse experiment by manipulating Argentine ant (Linepithema humile Mayr) colony size while holding constant the initial size of aphid (Chaitophorus populicola Thomas) aggregations. The two parameters associated with survival, aphid survivorship to maturity and longevity, declined with increasing tending intensity, whereas per capita birth rate and time to first reproduction showed no relationship to attendance. The intrinsic rate of increase declined only at relatively high tending levels, suggesting a nonlinearity in the effect of tending intensity. 3. Tending intensity measured in the experiment was similar to that observed in free‐living aggregations of C. populicola. Furthermore, the per capita recruitment rate of ants to free‐living aphid aggregations was negatively density‐dependent, indicating that small aggregations tend to experience the highest levels of tending intensity. This finding suggests that the aphid's intrinsic rate of increase may be positively density‐dependent, mediated by the aphid's mutualistic interaction with the ant. 4. In the Argentine ant–C. populicola interaction, experimental manipulation of colony size revealed a direct cost of ant attendance that was conditional upon tending intensity. Experiments that manipulate only ant presence or absence may yield an incomplete understanding of the mutualistic interaction if underlying nonlinearities exist.