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.     

Leaf surface wax and plant morphology of peas influence insect density

Insect predators and parasitoids adhere better, forage more effectively, and take more aphid prey on pea plants (Pisum sativum L.) (Leguminosae) with mutations that reduce the crystalline wax bloom on the plant surface. To assess the agronomic potential of this trait for pest management, abundance of pea aphids (Acyrthosiphon pisum L.) (Homoptera: Aphididae) and coccinellid predators, and percent parasitism of the aphids were evaluated on pea lines differing in wax bloom and plant architecture over two field seasons. Three pairs of pea lines were evaluated, each pair with a different architecture and differing within the pair in the amount of surface wax bloom (reduced or normal). The trials included plots treated with a narrow spectrum insecticide (pymetrozine) to reduce aphid populations and untreated controls. Reduced wax peas had significantly fewer aphids per plant in 2002 but not in 2003. Total natural enemy abundance was greater on reduced wax than on normal wax pea lines in both years of the study. Pymetrozine reduced aphid densities significantly in both years. Among the four pea lines evaluated for yield, seed yield per plant was affected by plant morphology and insecticide treatment. Yield was greatest on semileafless plants and on pymetrozine sprayed plots in both years. Yield of the reduced wax line in the semileafless background was similar to or exceeded yield in its normal wax sister line, suggesting that this morphological type was best for an agronomically viable reduced wax phenotype. Pea weevil (Bruchus pisorum L.) (Coleoptera: Bruchidae) damage to seed was overall more frequent on seeds from reduced wax varieties than from normal wax varieties. The results illustrate the trade‐offs associated with a reduced wax trait in peas but also show that certain combinations of reduced wax and gross morphology lead to reduced pea aphid populations and yields similar to those of normal wax peas.     

Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods

Abstract.  1. Although interactions between ants and honeydew-producing insects have received considerable study, relatively little is known about how these interactions alter the behaviour of ants in ways that affect other arthropods. In this study, field and greenhouse experiments were performed that examined how the presence of aphids ( Aphis fabae solanella ) on Solanum nigrum influenced the foraging behaviour of Argentine ants ( Linepithema humile ) and, in turn, modified the extent to which ants deter larval lacewings ( Chrysoperla rufilabris ), which are known aphid predators.
2. A field experiment demonstrated that the level of foliar foraging by ants increased linearly with aphid abundance, whereas no relationship existed between the level of ground foraging by ants and aphid abundance.
3. In the greenhouse, as in the field, foliar foraging by ants greatly increased when aphids were present. Higher levels of foliar foraging led to a twofold increase in the likelihood that ants contacted aphid predators. As a result of these increased encounters with ants, lacewing larvae were twice as likely to be removed from plants with aphids compared with plants without aphids. Once contact was made, however, the behaviour of ants towards lacewing larvae appeared similar between the two experimental groups.
4. Argentine ants drive away or prey upon a diversity of arthropod predators and parasitoids, but they also exhibit aggression towards certain herbivores. Future work should attempt to quantify how the ecological effects that result from interactions between honeydew-producing insects and invasive ants, such as L. humile , differ from those that result from interactions between honeydew-producing insects and native ants.     

Field‐level effects of preventative management tactics on soybean aphids (Aphis glycines Matsumura) and their predators

A 2‐year field experiment was conducted in northern Illinois to evaluate the effects of host plant resistance and an insecticidal seed treatment (thiamethoxam) on soybean aphids, Aphis glycines Matsumura and their predators. Densities of soybean aphids varied between the 2 years of the experiment. During both years, resistant plants experienced fewer cumulative aphid days than susceptible plants. Populations of soybean aphids on resistant plants rarely exceeded the economic injury level of 250 soybean aphids per plant. The use of thiamethoxam reduced cumulative aphid days in 2007, but not in 2008. Although soybean aphids reached densities that were sufficient to cause yield‐loss for untreated and susceptible plants, no yield‐benefit was associated with using the two management tactics in either year. This latter finding suggests that densities of soybean aphids need to be greater and sustained for a longer period of time than what we observed if the two management tactics are expected to provide a yield‐benefit. Monitoring natural enemies revealed that densities of key aphidophagous predators were relatively unaffected by host plant resistance or thiamethoxam; the effect of these management tactics on densities of predators, as well as the effectiveness of the method used to sample predators, is discussed.     

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.

     

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.     

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.     

Echinacea angustifolia and its specialist ant‐tended aphid: a multi‐year study of manipulated and naturally‐occurring aphid infestation

1. The impact of herbivores on plant fitness depends on multiple ecological mechanisms, including interactions between herbivore guilds. 2. This study assessed the effects of a specialist aphid (Aphis echinaceae) on performance and foliar herbivore damage of a long‐lived perennial plant (Echinacea angustifolia) native to the North American tallgrass prairie. A 2‐year field experiment manipulating aphid infestation on 100 plants was compared with concurrent and past observations of unmanipulated plants in the same outdoor experimental plot. Because ants co‐occur with aphids, the experiment tested the combined effects of aphids and ants. 3. Neither manipulated nor naturally‐occurring aphid infestations led to measurable declines in plant performance. Results for foliar herbivore damage differed between experimental and observational studies: the occurrence of foliar herbivore damage decreased with aphid infestation in the first year of the experiment and increased with aphid infestation over 5 years in unmanipulated plants. 4. While the experimental results concur with other experiments of ant–hemipteran–herbivore relationships, the observational results suggest that ant–aphid interactions do not naturally play a major role in determining patterns of foliar herbivory in this system. This result demonstrates the value of using field observations to interpret the relevance of experimental results.     

Effects of habitat fragmentation on the three-way interaction among ants,aphids and larvae of the giant purple emperor, <Emphasis Type="Italic">Sasakia charonda</Emphasis> (Hewitson), a near-threatened butterfly

Survival rates of both early and middle instar larvae of the nymphalid butterfly, Sasakia charonda, were estimated to be lowest on test trees planted in a meadow (site A), intermediate in a small, narrow secondary deciduous broadleaf forest (small patch, site B) and highest in a large secondary deciduous broadleaf forest (large forest, site C). The larval mortality rates due to predation by tree-climbing predators from the ground (tree climbing predator) such as ants and the larvae of carabids were estimated to be greater at sites A and B than those at site C. The number of predatory ants climbing test trees was significantly greater at sites A and B than at site C, and the ants harvested honeydew from aphids living on tree leaves at those two sites. Aphid densities were significantly higher on trees at sites A and B than at site C, and aphid densities and numbers of predatory ants were significantly and positively correlated at sites A and B. In an experiment controlling aphid density per branch on test trees, the numbers of ants and the mortality rates of S. charonda larvae were greater on branches with high aphid densities than on those with low aphid densities at both sites A and B. These results suggest that the aphid density per host tree was higher in the meadow and the small patch than in the large forest; at both sites these higher aphid densities attracted higher numbers of predatory ants to test trees, and as a result, mortality rates of S. charonda larvae were increased.     

Larvae of the green lacewing <Emphasis Type="Italic">Mallada desjardinsi</Emphasis> (Neuroptera: Chrysopidae) protect themselves against aphid-tending ants by carrying dead aphids on their backs

Larvae of the green lacewing Mallada desjardinsi Navas are known to place dead aphids on their backs. To clarify the protective role of the carried dead aphids against ants and the advantages of carrying them for lacewing larvae on ant-tended aphid colonies, we carried out some laboratory experiments. In experiments that exposed lacewing larvae to ants, approximately 40% of the larvae without dead aphids were killed by ants, whereas no larvae carrying dead aphids were killed. The presence of the dead aphids did not affect the attack frequency of the ants. When we introduced the lacewing larvae onto plants colonized by ant-tended aphids, larvae with dead aphids stayed for longer on the plants and preyed on more aphids than larvae without dead aphids. Furthermore, the lacewing larvae with dead aphids were attacked less by ants than larvae without dead aphids. It is suggested that the presence of the dead aphids provides physical protection and attenuates ant aggression toward lacewing larvae on ant-tended aphid colonies.     

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

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Population distribution and density of Pentalonia nigronervosa (Hemiptera: Aphididae) within banana mats: influence of plant age and height on sampling and management

The banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae), is the most economically important pest of banana (Musa spp.) fields in Hawaii. Recently, there has been a concerted effort in Hawaii to learn more about the biology and ecology of this pest. However, limited work has been directed at determining the distribution of P. nigronervosa in banana fields and developing an integrated pest management plan. Therefore, a survey was conducted in banana fields throughout the Hawaiian Islands to determine the distribution and density of P. nigronervosa within banana mats from plants of different stages. Another aim was to determine whether the presence of ants on banana plants could be used as a reliable indicator of aphid infestations. Results of the survey showed that plants < or = 1.5 m (small sucker) in height contain the highest aphid populations per meter in plant height and that mother plants (> or = 2.5 m) had the lowest aphid counts and rate of infestation compared with small and intermediate suckers (> 1.5 < 2.5 m). More specifically, aphid population was reduced by approximately 12 aphids for every meter increase in plant height and that aphids are rarely found > or = 2.5 m within the plant canopy. Although there was an increase likelihood of finding ants on banana plants with higher aphid densities, results suggest that ants would be present on plants in the absence of aphids. Implications of these and other findings with respect to sampling and managing P. nigronervosa and associated Banana bunchy top virus are discussed.     

Plant-aphid interactions: molecular and ecological perspectives

Many aphids are major agricultural pests because of their unparalleled reproductive capacity and their ability to manipulate host plant physiology. Aphid population growth and its impact on plant fitness are strongly influenced by interactions with other organisms, including plant pathogens, endophytes, aphid endosymbionts, predators, parasitoids, ants, and other herbivores. Numerous molecular and genomic resources have recently been developed to identify sources of aphid resistance in plants, as well as potentially novel targets for control in aphids. Moreover, the same model systems that are used to explore direct molecular interactions between plants and aphids can be utilized to study the ecological context in which they occur.     

Nutrient dynamics in a tritrophic system of ants,aphids and beans

The interactions between ants (Lasius niger), aphids (Aphis fabae) and plants (Phaseolus vulgaris) were studied in a laboratory experiment with the following treatments: application of N‐fertilizer for plants, supply of mealworms or sugar solution or their combination as alternative food sources for ants. Three main questions were studied: (1) Do ants reduce tending to honeydew‐producing aphids when an alternative sugar or protein resource was available? (2) Is aphid predation/protein consumption by ants higher when additional carbon is offered to maintain the carbon/protein balance? (3) Does fertilizer treatment propagate in the food web? For the experimental analysis stable isotope techniques were applied. δ¹⁵N served as a marker for the pathway from plants to higher trophic levels. Low δ¹⁵N‐value of fertilizer spread from plant shoots to aphids and ants. To trace which sugar‐/protein source was consumed by ants, the different ¹³C/¹²C‐ratios of C₃‐ and C₄‐plants were used with aphids feeding on C₃‐plant material, while mealworm food and sugar solution originated from C₄‐plant material. Fertilizer application had no effect on biomasses of plants, consumers or microflora. Ant biomass was significantly higher when additional sugar solution was offered. Higher contents of ¹³C indicated a high incorporation rate of additional sugar. Additional protein had no effect on colony biomass and no increasing predation on aphids could be observed when carbon was in excess. However, due to the lack of queens and newly produced larvae, protein requirements of experimental colonies were lower than in natural systems. Ants positively affected aphid populations, but reduced tending, whilst having access to an alternative sugar resource. When sugar/protein was offered to ants, the host plant had an increased root/shoot ratio. This indicates that decreasing aboveground activity of ants could lead to reduced plant growth of aphid‐infested plants, presumably due to higher fungal attack on shoots.     

Syrphid flies suppress lettuce aphids

Syrphid flies are abundant in lettuce fields, where their larvae are key predators of aphids. However, the presence of predators in the field does not always result in economically significant levels of prey suppression. Even when predators are numerous, their effects on prey population dynamics may be variable. Over a two year period we surveyed lettuce fields in coastal California, USA to test whether syrphid flies are capable of colonizing fields with aphids and suppressing aphid population growth. The survey showed that female syrphids oviposited more eggs at locations with more aphids, and that greater numbers of syrphid larvae resulted in lower rates of increase in the aphid populations. We also directly manipulated syrphid densities by adding syrphid eggs to uncaged lettuce plants, and these syrphid additions resulted in lower aphid population growth. This research shows that syrphid flies have the ability to suppress aphid populations in lettuce fields.     

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.     

Habitat variation,mutualism and predation shape the spatio‐temporal dynamics of tansy aphids

1. Spatially distributed resources can lead to the formation of metapopulations, where individual subpopulations are often small and can experience frequent local extinction events followed by recolonisation. An example of terrestrial metapopulations are specialised phytophagous insects on their patchily distributed host plants. 2. The present study investigated the population dynamics of a specialised aphid (Metopeurum fuscoviride) on its patchily distributed host plant (Tanacetum vulgare) and associated community of mutualistic ants and predators in a small‐scale field site. Furthermore, aphid habitat differences (plant size, C/N ratio, location and surrounding vegetation) were quantified, and seasonal timing and precipitation were considered. 3. Seasonal timing and precipitation both had effects on aphid colonisation, extinction events and aphid colony persistence. Towards the end of the season, and after higher precipitation, aphid colonisation events decreased and extinction events increased. Plant size and location as well as aphid within‐field dispersal determined the spatio‐temporal distribution of aphid colonies. 4. Mutualistic ants (Lasius niger and Myrmica rubra) increased the chance of establishment of aphid colonies. However, when M. rubra was tending, aphid colony persistence was reduced. Aphid persistence and extinction were dependent on aphid abundance, as a higher colony size reduced the probability of extinction by predation. 5. The results emphasise the importance of dispersal limitation, population growth and the presence of mutualists when studying the spatio‐temporal dynamics of tansy aphids, particularly in a small‐scale field site.     

Effect of hunger on the allocation of time among pea plants by the larvae of an aphidophagous hover fly,Eupeodes corollae [Dipt: Syrphidae]

We observed the movement of predatory larvae of the syrphid flyEupeodes corollae (F.) (formerlyMetasyrphus corollae) among small pea plants with and without aphids. Starved larvae spent longer time than well-fed larvae on similar plants and both groups of larvae stayed longer on plants with aphids than on plants without aphids. On plants with aphids, larvae which failed to capture prey left the plant sooner than those which captured aphids. The capture of at least one aphid on a plant increased the persistence of syrphid larvae. The average rate of energy gain was higher for well-fed larvae than for starved larvae because starved larvac stayed on plants even when their rate of return was lower. When larvae that had captured aphids left plants, their rate of energy gain, tended to be lower than at any time following capture of the 2^nd, aphid. The 1^st aphid was captured in less time than similar larvae spent on plants without aphids. Time between captures of aphids by well-fed larvae was less than the time such larvae spent on plants without aphids. Among starved larvae, the intercatch intervals were similar to the time on plants without aphids. We discuss the significance of these results relative to current predator foraging theory and the efficiency ofE. corollae as a biological control agent.      

Genetically based population variation in aphid association with ants and predators

A species’ genotype can have extended consequences for the structure of the surrounding community, but few studies have investigated the extended consequences of genetic variation in animals. Accordingly, I examined the importance of genetically based variation among five populations of the ant-tended aphid Aphis asclepiadis for its interactions with both ants and predators. In a common environment, aphid source population accounted for 23 and 17% of the variation in the occurrence of ants and predators, respectively. Ant exclusion increased predator abundance, accounting for 25% of variation, but there was no detectable influence of ants on aphid abundance. There was an indication that aphid source populations varied in honeydew quality, but this was uncorrelated with rates of ant attendance. This study provides the first evidence for genetic variation in aphids for attractiveness to ants, and underscores the important link between intra-specific genetic variation in aphids and the processes governing arthropod community structure.     

Influence of aphid honeydew on the foraging behaviour of Hippodamia convergens larvae

1. Environmental cues associated with prey are known to increase predator foraging efficiency. Ladybird larvae are major predators of aphids. The sugary excretion of aphids (honeydew) has been proposed to serve as a prey‐associated cue for ladybird larvae. 2. Ladybird larvae are regularly found on the ground moving between plants or after falling off plants. The use of prey‐associated cues would be particularly beneficial for ladybird larvae on the ground in that such cues would help them to decide which plants to climb because aphids are patchily distributed within as well as amongst plants and, as a result, many plants are either not infested with aphids or do not host an aphid species of high nutritional value for ladybird larvae. 3. Laboratory experiments with larvae of Hippodamia convergens Guérin‐Méneville (Coleoptera: Coccinellidae) were carried out to explore whether honeydew accumulated on the ground is used as a foraging cue. The study also investigated whether, if honeydew is a foraging cue, larvae show differential responses to honeydew of high‐quality prey Acyrthosiphon pisum Harris compared with that of low‐quality prey Aphis fabae Scopoli (both: Homoptera: Aphididae). 4. Hippodamia convergens larvae stayed longer in areas containing honeydew but did not engage in longer bouts of searching. Furthermore, larvae did not distinguish between honeydew from high‐ and low‐quality aphid prey.