Should aphids attract or repel ants? Effect of rival aphids and extrafloral nectaries on ant–aphid interactions

Among plants and herbivores, two types of conflicts occur in relation to mutualism with ants: one is competition for ant mutualism among myrmecophilous herbivores and plants, and the other is the conflict whether to attract or repel ants between myrmecophiles and nonmyrmecophiles that are damaged by ants. We investigated the extent to which two species of aphids (Megoura crassicauda and Aphis craccivora) and extrafloral nectaries on their host plant (Vicia faba var. minor) interact with one another for their relationships with ants. We designed an experiment where ants can choose to visit seedlings colonized by (1) M. crassicauda, (2) A. cracivora, (3) both aphid species, or (4) neither aphid species. Ants preferred A. craccivora to extrafloral nectaries and avoided tending M. crassicauda. We also analyzed the population growth of each aphid when it coexists with (1) ants, (2) the other aphid species, (3) ants and the other aphid species, or (4) neither of them. Under ant-free conditions, we detected an exploitative competition between the two aphid species. The ants had no significant effect on the population of A. craccivora, whereas they had negative effects on the population growth of M. crassicauda by attacking some individuals. When both aphids coexisted, M. crassicauda suffered ant attack more intensely because A. craccivora attracted more ants than extrafloral nectaries despite ant-repelling by M. crassicauda. On the other hand, the ants benefited A. craccivora by eliminating its competitor. To avoid ant attack, aphids may have been selected either to be more attractive to ants than other sympatric sugar sources or to repel the ants attracted to them. We hypothesize that competition among sympatric sugar sources including rival aphids and extrafloral nectaries is a factor restricting aphids to be myrmecophilous. Received: January 17, 2000 / Accepted: July 4, 2000     

Oviposition behaviour of the aphid parasitoid,Aphidius ervi: Are wet aphids recognized as host?

Females of the central European population of the aphid parasitoid, Aphidius ervi, did not attack wet pea aphids (Acyrthosiphon pisum) that were washed previously with water. After 1 hour, this phenomenon disappeared and A. ervi attacked washed hosts to the same degree as dry ones. Similarly, A. ervi attacked dead aphids killed in liquid nitrogen readily if they were dry but not if they were wet. This effect was also reversible and disappeared after 1 h. When A. ervi females were foraging on broad beans (Vicia faba), they laid significantly more eggs into dry aphids than into wet aphids. Resource utilization of wet aphids, however, was significantly lower in this design than in Petri dishes, due to a changed drop-off behaviour of the aphid. We conclude that females did not use visual cues for host recognition but instead relied on chemical cues. These cues may be covered by a thin water layer directly after aphids became wet. Our results also demonstrate the importance of abiotic factors for the estimation of the reproductive success of parasitoids in the field.     

Interaction of ants with aphid enemies: Do inexperienced ants specializing in honeydew collection recognize aphidophages at their first contact?

Honeydew collectors of Formica pratensis taken from the nature (control) and laboratory-reared “naïve” ants, which had never met either “mature” workers or aphids and aphidophages, were observed during their interactions with various aphid enemies: adults and larvae of ladybirds and lacewings, and larvae of syrphid flies. The naïve ants were significantly more aggressive towards adults than towards larvae of aphidophages. More than 70% of the naïve ants treated ladybirds and lacewings as enemies at their first encounter and attacked them immediately without any prior antennation. The frequency of aggressive reactions (body jerking and bites) towards larvae was significantly higher in the control group, whereas the percentage of ants showing explorative behavior was significantly higher in the naïve ants. Overall, experience proved to be not important for displaying the key behavioral reactions towards adult ladybirds and lacewings underlying the protection of trophobionts from these natural enemies. However, accumulation of experience is assumed to play an important role in the recognition of aphidophage larvae and formation of aggressive behavior towards them.     

Are ant-aphid associations a tritrophic interaction? Oleander aphids and Argentine ants

Summary Oleander aphids, (Aphis nerii), which are sporadically tended by ants, were used as a moded system to examine whether host plant factors associated with feeding site influenced the formation of ant-aphid associations. Seasonal patterns of host plant utilization and association with attendant ants were examined through bi-weekly censuses of the aphid population feeding on thirty ornamental oleander plands (Nerium oleander) in northern California in 1985 and 1986. Colonies occurred on both developing and senescing plant terminals, including leaf tips, floral structures, and pods. Aphids preferentially colonized leaf terminals early in the season, but showed no preference for feeding site during later periods. Argentine ants (Iridomyrmex humilis) occasionally tended aphid colonies. Colonies on floral tips were three to four times more likely to attract ants than colonies on leaf tips, even though the latter frequently contained more aphids. Ants showed a positive recruitment response to colonies on floral tips, with a significant correlation between colony size and number of ants. There was no recruitment response to colonies on leaf tips. These patterns were reproducible over two years despite large fluctuations in both aphid population density and ant activity. In a laboratory bioassay of aphid palatability, the generalist predator,Hippodamia convergens, took significantly more aphids reared on floral tips compared to those reared on leaf tips. The patterns reported here support the hypothesis that tritrophic factors may be important in modifying higher level arthropod mutualisms.     

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

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

Ant attendance in aphids: why different degrees of myrmecophily?

1. Aphids show a range of associations with ants from nonattendance to obligate myrmecophily. Aphis fabae cirsiiacanthoides is facultatively associated with ants, while Symydobius oblongus is an obligate myrmecophile. The selection pressures that have shaped these associations are unknown. 2. The consequences for these aphids of their different degrees of associations with ants were determined, in terms of costs and benefits to individuals and colonies in laboratory and field experiments. In the laboratory, individuals of A. f. cirsiiacanthoides performed worse and those of Symydobius oblongus performed better when attended by the ant Lasius niger than when unattended. For example, when ant-attended, A. f. cirsiiacanthoides developed more slowly, were smaller, and invested less in gonads, whereas S. oblongus developed more quickly, were larger, and invested more in gonads. In addition, the ant regulated the population size of S. oblongus to an average of 50–70 individuals per birch sapling by removing aphids, but did not regulate the population size of A. f. cirsiiacanthoides. 3. Under field conditions, ant-attended colonies of both A. f. cirsiiacanthoides and S. oblongus achieved higher peak numbers and lasted longer, and ant-attended colonies of A. f. cirsiiacanthoides produced more alate dispersers than unattended colonies. 4. The implications of divergent selection pressures for the development of myrmecophily in aphids are discussed.     

Spatial organization in ants’ nests: does starvation modify the aggregative behaviour of Lasius niger species?

Ant colonies that undergo long starvation periods have to tune their exploratory and foraging responses to face their food needs. Although the number of foragers is known to increase with food deprivation in the ant Lasius niger, such enhanced food exploitation is not related to a more intense recruitment by successful scouts. We thus suggest that the colony’s response to a food shortage could result from changes at the level of the ant recruits, in particular from changes in their spatial organization inside the nest. Since aggregation plays a key role in the social organization of ants, we assume that the colony’s response to starvation could be due to changes in the aggregative behaviour of L. niger nestmates.We thus compared the aggregation dynamics of inner-nest workers and foragers having undergone either a short or a long-lasting starvation period. Whatever the ethological group (foragers or inner-nest workers), there was no significant influence of starvation on the aggregation dynamics nor on any feature of the observed clusters. This result shows that an increased foraging response to food shortage cannot be explained by changes in the tendency of nestmates to aggregate within the nest. Finally, we discuss other behavioural mechanisms, in particular changes in behavioural thresholds that could underlie the adaptive changes seen in colony foraging after long starvation periods. Received 25 June 2007; revised 21 January 2008; accepted 24 January 2008.     

Congruency of hydrocarbon patterns in heterospecific groups of ants: transfer and/or biosynthesis?

Summary In homospecific groups of ants, each species has its own hydrocarbon profile, on the epicuticle and in the postpharyngeal gland (PPG). When reared together in bispecific groups, workers of both species possess each other's hydrocarbons in both locations. The present study investigated two alternative mechanisms by which a mixed odour in artificial groups ofFormica selysi/Manica rubida can be created. Using [1-¹⁴C] sodium acetate as a precursor,de novo biosynthesis of hydrocarbons was demonstrated for both species whether reared in homospecific or mixed-species groups. The newly synthesized hydrocarbons occurred on the epicuticle, internally, and in particularly large amounts in the PPG. As expected from their PPG and epicuticular hydrocarbons composition, workersF. selysi synthesized alkanes and alkenes in comparable amounts irrespective of their rearing scheme. Likewise,M. rubida reared in bispecific groups synthesized mostly alkanes with only negligible amounts of alkenes, according to a ratio characteristic toM. rubida workers from homospecific groups and not toF. selysi workers. During dyadic encounters, a transfer of labeled hydrocarbons between nestmates (conspecific in homospecific groups and allospecific in mixed groups) was observed. These results suggest that the formation of the mixed hydrocarbon profile in artificial groups of ants is the result of a transfer of these chemicals between nestmates rather thande novo biosynthesis of the allospecific hydrocarbons. Behaviours like trophallaxis, grooming and body contact that occurred during the encounters mediated such a transfer.     

Is oral microbiome of children able to maintain resistance and functional stability in response to short-term interference of ingesta?

Dear Editor, A series of studies had focused on the ecological stability of human microbiome (Lozupone et al.,2012;Faith et al.,2013;Moya and Ferrer,2016).Despite the continuous perturbation and the highly personalized composition within the human microbiome (Human Microbiome Project,2012),healthy adults stably maintain their microbial communities in terms of space and time (Faith et al.,2013;Moya and Ferrer,2016;Oh et al.,2016).This stability is proved to be critical for the well-being of human body (Lozupone et al.,2012).On the contrary,major shifts in microbial community composition are often related to diseases (Lynch and Pedersen,2016).     

Mating behaviour in Schistosomes: are paired worms always faithful?

Previously assumed to be monogamous, the mating system of schistosomes has been the subject of some debate since recent findings have shown that change of mate can occur among these parasites. Here, Louis-Albert Tchuem Tchuenté, Vaughan R. Southgate, Claude Combes and Joseph Jourdane review progress made in the understanding of the mating behaviour of schistosomes, and highlight the importance of mating systems in the dynamics of natural transmission of schistosomiasis.     

Are developing beta-adrenoceptors able to desensitize? Acute and chronic effects of beta-agonists in neonatal heart and liver

During fetal and neonatal development, beta-adrenergic receptors (beta-ARs) appear to be resistant to desensitization by beta-agonist drugs. To determine the mechanisms underlying the regulatory differences between adults and neonates, we administered isoproterenol, a mixed beta(1)/beta(2)-AR agonist, and terbutaline, a beta(2)-selective agonist. Effects were examined in the ensuing 4 h after a single injection, or after the last of four daily injections. We prepared cell membranes from heart (predominantly beta(1)-ARs) and liver (predominantly beta(2)-ARs) and assessed signal transduction in the adenylyl cyclase (AC) pathway. In the first few hours after a single administration of isoproterenol to adult rats, cardiac beta-ARs showed activation of G proteins (elevated AC response to forskolin) and desensitization of beta-AR-mediated responses; after the fourth injection, heterologous desensitization emerged, characterized by a loss of signaling mediated either through beta-ARs or glucagon receptors. Terbutaline evoked an increase in the forskolin response but no desensitization of receptor-mediated responses. When we gave the same treatments to neonatal rats, we observed cardiac G protein activation, but there was neither homologous nor heterologous desensitization of beta-ARs or glucagon receptors. In the adult liver, isoproterenol and terbutaline both failed to evoke desensitization, regardless of whether the drugs were given once or for 4 days. In neonates, however, acute or chronic treatment elicited homologous desensitization of beta-AR-mediated AC signaling, while sensitizing the response to glucagon. These results show that neonatal beta-ARs are inherently capable of desensitization in some, but not all, cell types; cellular responses can be maintained through heterologous sensitization of signaling proteins downstream from the receptor. Differences from adult patterns of response are highly tissue selective and are likely to depend on ontogenetic differences in subtypes of beta-ARs and AC.     

Cholinesterases of aphids—II: Anticholinesterase potency and toxicity of different organophosphorous inhibitors for spring grain aphid Schizaphis gramina rond

Anticholinesterase potency and toxicity for spring grain aphids of 52 organophosphorous inhibitors (OPI) of different structures were investigated. As regards sensitivity to OPI, the acetylcholinesterase (AChE) and butyrylcholinesterase (BuChE) of the spring grain aphid are shown to differ significantly from the “typical” cholinesterases, i.e. from human erythrocyte AChE and horse serum BuChE, which is presumably associated with differences in the structures of the active surface of these enzymes. The extremely high sensitivity of spring grain aphid AChE to cationic OPI containing the onium atom in the leaving part of the molecule indicates the fundamental importance of the anionic site in the active centre of the enzyme. By contrast, spring grain aphid BuChE has low sensitivity to OPI, typical of the cationic type, which suggests that it has no anionic site. Correlation was established between the toxicity and anticholinesterase potency of OPI which contain no cationic groups or bulky hydrophobic radicals.     

Is the response of aphids to alarm pheromone stable?

Aphid taxa are characterized by a number of biological features, such as their feeding behaviour and host selection, which it is generally accepted are affected by keeping them for several generations under standard conditions in a laboratory. Analyses of three strains of the green pea aphid, Acyrthosiphon pisum (Harris, 1776), reared in culture for long periods, indicate that other characters are also affected. For example, the response of these aphids to alarm pheromone is dramatically reduced. This raises an interesting question regarding the mechanism by which it occurs and has consequences when aphids from laboratory cultures are used for studies in ecology and applied biology and especially the long‐term effectiveness of crop plants genetically engineered to produce EBF as a means of controlling aphids.     

Using fossils to determine an amber source: aphids and crane flies in Chinese or Baltic amber?

Aphids and crane flies in amber purported to have originated in China were examined. Six aphid specimens were characterised and determined to be conspecific with Germaraphis defuncta Heie, originally described from Baltic amber. Two crane flies from the same collection were identified as Cheilotrichia minuta and Rhabdomastix brevis, species also previously described from Baltic amber. This study shows that when the locality of an amber source is ambiguous, fossils can be used to determine the true province.     

Worker brain development and colony organization in ants: Does division of labor influence neuroplasticity?

Brain compartment size allometries may adaptively reflect cognitive needs associated with behavioral development and ecology. Ants provide an informative system to study the relationship of neural architecture and development because worker tasks and sensory inputs may change with age. Additionally, tasks may be divided among morphologically and behaviorally differentiated worker groups (subcastes), reducing repertoire size through specialization and aligning brain structure with task‐specific cognitive requirements. We hypothesized that division of labor may decrease developmental neuroplasticity in workers due to the apparently limited behavioral flexibility associated with task specialization. To test this hypothesis, we compared macroscopic and cellular neuroanatomy in two ant sister clades with striking contrasts in worker morphological differentiation and colony‐level social organization: Oecophylla smaragdina , a socially complex species with large colonies and behaviorally distinct dimorphic workers, and Formica subsericea , a socially basic species with small colonies containing monomorphic workers. We quantified volumes of functionally distinct brain compartments in newly eclosed and mature workers and measured the effects of visual experience on synaptic complex (microglomeruli) organization in the mushroom bodies—regions of higher‐order sensory integration—to determine the extent of experience‐dependent neuroplasticity. We demonstrate that, contrary to our hypothesis, O. smaragdina workers have significant age‐related volume increases and synaptic reorganization in the mushroom bodies, whereas F. subsericea workers have reduced age‐related neuroplasticity. We also found no visual experience‐dependent synaptic reorganization in either species. Our findings thus suggest that changes in the mushroom body with age are associated with division of labor, and therefore social complexity, in ants. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1072–1085, 2017     

Feeding and foraging behaviour of a generalist caterpillar: are third instars just bigger versions of firsts?

Similarities and differences in foraging behaviour between first and third instar Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on Vigna radiata (L.) R. Wilczek (Fabaceae) (mung bean) were determined by frequent, repeated observation of insects on whole plants. The time apportioned to feeding, resting and searching by these two larval instars differed. Third instars were often found feeding on exposed areas of the plant and, if in the terminal parts, would leave these areas more frequently than first instars. Third instars fed at fewer sites and spent less time searching and resting, fed in longer bouts and spent 20% more time feeding than first instars. Although both instars tended to move upwards to the top of the plant, this applied to approximately half of the third instars observed compared to all of the first instars. First instars were found to have a higher relative growth rate than third instars. The results show that it cannot be assumed that first instars are just smaller versions of late instars.     

Nestmate recognition in Camponotus floridanus callow worker ants: are sisters or nestmates recognized?

Callow workers of the Florida carpenter ant, Camponotus floridanus Buckley, reared with their sisters displayed more aggressive acts towards unrelated unfamiliar foragers than towards related unfamiliar foragers. When callows were reared with foreign nurses they were more aggressive towards their own unfamiliar sisters than towards the unfamiliar sisters of their nurses. Thus callow workers recognized the sisters of the workers they were reared with as nestmates. This ability was not dependent on whether or not callows received cues from older ants during their emergence. Similarly, a forager was less aggressive towards unfamiliar callows reared with its sisters than towards those reared with nurses unrelated to itself. In addition, foragers were less aggressive towards their callow sisters than towards unrelated callows, regardless of the relatedness between the foragers and the rearing nurses.     

Plasmolysis bays in Escherichia coli: are they related to development and positioning of division sites?

Plasmolysis bays, induced in Escherichia coli by hypertonic treatment, are flanked by zones of adhesion between the plasma membrane and the cell wall. To test the proposition of Cook et al. (W. R. Cook, F. Joseleau-Petit, T. J. MacAlister, and L. I. Rothfield, Proc. Natl. Acad. Sci. USA 84:7144-7148, 1987) that these zones, called periseptal annuli, play a role in determining the division site, we analyzed the positions of these zones by phase-contrast and electron microscopy. In situ treatment of cells grown in agar showed that the youngest cell pole was the most susceptible to plasmolysis, whereas the constriction site was resistant. Lateral bays occurred only at some distance from a polar bay or a resistant constriction site. Orienting cells with their most prominently plasmolyzed polar bay in one direction showed that the lateral bays were always displaced away from the polar bay at about half the distance to the other cell pole. If no poles were plasmolyzed, lateral bays occurred either in the centers of nonconstricting cells or at the 1/4 or 3/4 position of cell length in constricting cells. The asymmetric positions of lateral plasmolysis bays, caused by their abrupt displacement in the presence of polar bays or constriction sites, does not confirm the periseptal annulus model (Cook et al.), which predicts a gradual and symmetric change in the position of lateral bays with increasing cell length. Our analysis indicates that plasmolysis bays have no relation to the development and positioning of the future division site.