Behavioral strategies of aphid hyperparasitoids to escape aggression by honeydew-collecting ants

We analyzed the behavioral interactions between two species of honeydew-collecting ants (Lasius niger, Myrmica laevinodis) and foraging females of four species of aphid hyperparasitoids (Aphidencyrtus aphidivorus, Dendrocerus carpenteri, Pachyneuron aphidis, Asaphes vulgaris) usingAphis fabae ssp.cirsiiacanthoidis andLysiphlebus cardui on thistles as aphid and primary parasitoid, respectively. The observed interaction patterns and foraging parameters varied within hyperparasitoid species and revealed different strategies based upon behavioral and morphological constraints.D. carpenteri generally tried to avoid ant encounters. This avoidance strategy was successful in interactions withM. laevinodis but failed when encountering the more aggressiveL. niger, which caused about 26% adult mortality. In contrast,A. aphidivorus, P. aphidis, andA. vulgaris possess jumping ability and were hardly exposed to mortality risks. The escape reaction jump off was used as soon as ants made physical contact with foraging females. While the flight strategy ofP. aphidis is connected with cryptic movement patterns without avoidance behavior,A. aphidivorus first avoided ants and jumped off only as a last resort. Similar patterns, but less expressive, are displayed byA. vulgaris. We suggest that these different strategies are responsible for different foraging success in ant-attended resources in field.     

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.     

Larvicidal activity of lectins onLucilia cuprina: mechanism of action

Foraging behaviour and host-instar preference of young and old females of the solitary aphid parasitoid,Lysiphlebus cardui Marshall (Hymenoptera: Aphidiidae), were studied in the laboratory. The analysis of interactions between parasitoids and different stages ofAphis fabae cirsiiacanthoidis Scop. (Homoptera: Aphididae) revealed that encounter rates between aphids and parasitoid females and defence reactions of the aphids influenced the degree to which a particular aphid age class is parasitized. Encounter rates between hosts and parasitoid females depended on the foraging pattern of the parasitoid, which varied with age. In mixed aphid colonies patch residence time increased with parasitoid age. Furthermore, younger parasitoids (≦1 day old) laid more eggs into second and third instars, while older parasitoids (≧4 days old) did not show distinct host instar preferences. It is suggested that the oviposition behaviour ofL. cardui is influenced by the physiological state, i.e. the age of the wasp.     

Success of aphid parasitoids and their hosts varies with ant attendance: A field study

Aphid–ant associations are often described as mutually beneficial interactions in which honeydew is traded for protection from predators and parasitoids. The aim of the present study was to determine parasitization avoidance in ant‐tended aphid colonies. Field experiments were carried out on two host plants: hoary cress Lepidium draba (Brassicaceae) and Canadian teasel Cirsium arvense (Asteraceae). Lepidium was host to Acyrthosiphon gossypii (Aphididae) tended by the ant Lasius turcicus (Formicidae) and attacked by two parasitoids, Trioxys asiaticus (Braconidae) and Lysiphlebus fabarum (Braconidae). Cirsium was host to Brachycaudus cardui tended by Crematogaster sordidula and attacked by L. fabarum and Aphidius colemani (Braconidae). The per capita population growth rate of A. gossypii was significantly higher in the presence of ants, while B. cardui was negatively affected, albeit non‐significantly. The parasitism rate of A. gossypii decreased significantly when tended by Lasius turcicus, but the presence of Crematogaster sordidula in colonies of B. cardui significantly increased parasitism. Our results indicate that the effects of ant attendance vary between different aphid–ant interactions. Moreover, parasitoids can benefit from the presence of ants under some conditions.     

Differential Interactions Between an Aphid Endohyperparasitoid and Three Honeydew-Collecting Ant Species: A Field Study of Alloxysta brevis (Thomson) (Hymenoptera: Alloxystidae)

The behavioral interactions between the chemically protected aphid hyperparasitoid Alloxysta brevis and three trophobiotic ant species were examined in the field on thistles. The patterns were not essentially influenced by hyperparasitoid sex. Ants differed in their guarding behavior of aphids and their response toward A. brevis. Lasius niger attacked the hyperparasitoid more readily than Myrmica laevinodis, while aggression by Formica rufa was intermediate. Apart from applying chemical defense, A. brevis responded to ants by flying away (mainly at L. niger) or with avoidance behavior (mainly at M. laevinodis). Additionally, females might switch their tactics from flight to defense with increasing age. Females left the plant more often after encounters with L. niger or F. rufa than with M. laevinodis. Disturbance by any ant species affected the foraging activities, reducing oviposition success to nearly zero.     

Kairomonal effect of an aphid cornicle secretion onLysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae).

In laboratory bioassays, whole-body homogenates and fresh cornicle wax of Rhopalosiphum padi(L.) (the bird-cherry oat aphid) elicited antennal examination and attack behavior in naive females of the polyphagous aphidiid parasitoid, Lysiphlebus testaceipes (Cresson). No such response was elicited by either homogenates or cornicle wax of Aphis nerii(Boyer de Fonscolombe) (another known host of the parasitoid) or by preparations of the aphid alarm pheromone, (E)--farnesene. The response to R. padiproducts was independent of rearing host and appears to be innate. Application of R. padicornicle wax to the dorsum of a nonhost aphid [Acythosiphum pisum(Harris)] increased the frequency with which this species was attacked by L. testaceipes.There was a tendency for the kairomonal activity of the cornicle secretion to decline as the wax dried, although parasitoid attack behavior was still elicited by wax which had been allowed to dry for up to 30 min before testing.     

Memory and chemical communication in the orientation of two mass-recruiting ant species

Summary The relative contribution of visual and chemical components in the orientation ofLasius niger andIridomyrmex humilis (Argentine ant) workers during mass recruitment to newly discovered food sources is analyzed over short time intervals. While both species orient in response to the trail pheromone, a large number ofL. niger foragers rapidly switch to a more individual orientation, based on their memory of environmental cues.I. humilis workers, on the other hand, predominantly use collective chemical cues. The effect of the number of reinforcements on visual learning and its interference with chemical communication show that olfactory cues always prevail in the Argentine ant. InL. niger, the proportion of ants orienting to visual cues is independent of the trail concentration. Detailed observations of the trail-laying behavior of individually marked foragers show that nearly all theI. humilis workers initially lay a trail, whereas only half theL. niger foragers do so. This proportion decreases considerably with the number of trips performed byL. niger workers, while remaining constant for the Argentine ants. These results are interpreted with respect to the species' behavioral ecology.     

Adaptations of Coccinella magnifica Redtenbacher, a Myrmecophilous Coccinellid, to Aggression by Wood Ants (Formica rufa Group). I. Adult Behavioral Adaptation, Its Ecological Context and Evolution

Coccinella magnifica is an obligate associate of Formica rufa-group ants. The congener Coccinella septempunctata can serve as a model for its nonmyrmecophilous ancestor. Formica rufa behavior toward these two ladybirds, and their behavior, was compared. Although C. magnifica was rarely attacked on ant trails, it was usually attacked on tended aphid colonies. Coccinella septempunctata was more readily attacked. The two ladybirds' behavior was similar on trails, but C. magnifica used more defense and C. septempunctata more rapid escape behavior on aphid colonies. Only C. magnifica fed upon tended aphids. Chemical adaptation to overcome ant aggression probably exists in C. magnifica, but it possesses almost no novel behaviors to counter ant aggression. Instead, modifications have occurred in the expression of behaviors present in C. septempunctata.     

Hyperparasitoid defense strategies against spiders: the role of chemical and morphological protection

The aphid endohyperparasitoid Alloxysta brevis(Thomson) (Hymenoptera: Charipidae) applies defensive chemicals stored in mandibular gland reservoirs against attacking ants. Alloxystines can be divided into species capable of exploiting ant-attended resources and into species exclusively reared from unattended aphid-parasitoid systems. Mandibular secretions are found in species of both groups, with little variation in chemical composition. We show that the mandibular gland secretion does not only protect against ant attacks but acts as an overall defense agent against generalist predators like spiders. The protective success differed with the spider species. The web-building spider Agelena labyrinthica(Clerck) (Araneae: Agelinidae) killed 57% of attacked A. brevisfemales, but sucked out only 8%. The smaller free-hunting jumping spider Salticus scenicus(Clerck) (Araneae: Salticidae) failed in overwhelming or severely injuring A. brevis. The pattern of interactions showed striking similarities with interactions between A. brevisand the ant Lasius niger(Hymenoptera: Formicidae). Primary parasitoids which are lacking chemical defense and sufficient morphological protection suffered significantly higher mortality due to spider predation. Our results indicate that – additional to chemical defense- parasitoid survival depends on the specific morphological resistance against grip pressure during capture, and on the predator – prey size relationship.     

Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences

The honeydew composition and production of four aphid species feeding on Tanacetum vulgare, and mutualistic relationships with the ant Lasius niger were studied. In honeydew of Metopeurum fuscoviride and Brachycaudus cardui, xylose, glucose, fructose, sucrose, maltose, melezitose, and raffinose were detected. The proportion of trisaccharides (melezitose, raffinose) ranged between 20% and 35%. No trisaccharides were found in honeydew of Aphis fabae, and honeydew of Macrosiphoniella tanacetaria consisted of only xylose, glucose and sucrose. M. fuscoviride produced by far the largest amounts of honeydew per time unit (880 μg/aphid per hour), followed by B. cardui (223 μg/aphid per hour), A. fabae (133 μg/aphid per hour) and M. tanacetaria (46 μg/aphid per hour). The qualitative and quantitative honeydew production of the aphid species corresponded well with the observed attendance by L. niger. L. niger workers preferred trisaccharides over disaccharides and monosaccharides when these sugars were offered in choice tests. The results are consistent with the ants' preference for M. fuscoviride, which produced the largest amount of honeydew including a considerable proportion of the trisaccharides melezitose and raffinose. The preference of L. niger for B. cardui over A. fabae, both producing similar amounts of honeydew, may be explained by the presence of trisaccharides and the higher total sugar concentration in B. cardui honeydew. M. tanacetaria, which produced only low quantities of honeydew with no trisaccharides was not attended at all by L. niger. Received: 2 March 1998 / Accepted: 16 November 1998     

Honeydew collection by the invasive garden ant Lasius neglectus versus the native ant L. grandis

Honeydew collection performed by the invasive ant Lasius neglectus and by the native ant L. grandis was compared. The invasive ant collected 2.09 kg of honeydew per tree while the native ant collected 0.82 kg. The aphid Lachnus roboris was visited by both ant species. In holm oaks colonized by L. neglectus, aphid abundance tended to increase and its honeydew production increased twofold. The percentage of untended aphids was lower in holm trees occupied by L. neglectus. As tending ants also prey on insects, we estimated the percentage of carried insects. The native ant workers carried more insects than the invasive ant. Both ant species preyed mainly on Psocoptera and the rarely tended aphid, Hoplocallis picta. We conclude that the higher honeydew collection achieved by L. neglectus was the consequence of (1) its greater abundance, which enabled this ant to tend more Lachnus roboris and (2) its greater level of attention towards promoting an increase of honeydew production. Handling editor: Heikki Hokkanen     

The influence of ant-attendance on aphid behaviour investigated with the electrical penetration graph technique

For the mutualistic interaction between the aphid Metopeurum fuscoviride Stroyan (Homoptera: Aphididae) and the ant Lasius niger L. (Hymenoptera: Formicidae) it has been shown that ant-tended aphids develop faster, reproduce at a higher rate, and live longer than aphids not tended by ants. We used electrical penetration graphs (EPG) to investigate if behavioural patterns differ between ant-tended and untended M. fuscoviride during 8 h experiments. Measurements were made on adult aphids from four different ant-tended colonies that continued to be tended by L. niger during the experiments, and from four different colonies where ant workers were excluded several days before the start of the experiment and that were also not tended by ants during the experiments. Ants readily tended wired aphids and ant tending did not interfere with the EPG measurements. There were no significant differences in the duration of sieve element penetration or in any other analysed feeding-related EPG parameters between ant-tended and untended individuals. However, the quality of the EPG recordings did not allow the distinction between the EPG-waveform E1 (salivation only) and E2 (salivation and ingestion). These results suggest that the changes in life-history traits of ant-tended aphids do not result from changes in time of sieve element penetration waveforms. Alternative mechanisms may involve an increase in the rate of sap uptake or a higher effectiveness in nutrient uptake in the presence of ants. Our study demonstrates that the EPG technique is a useful tool to investigate the feeding behaviour of aphids during interactions with ants.     

Specificity of an ant-lycaenid interaction

Summary Many lycaenid butterflies are believed to be mutualists of ants — the butterfly larvae secrete sugars and amino acids as rewards for the ants, and the ants protect the larvae from predation or parasitism. We examined the specificity of the relationship between the lycaenid Plebejus argus and ants in the genus Lasius. Eggs were not attractive to Lasius ants until the emerging larvae had broken through the chorion. First instar larvae were palpated and picked up by Lasius workers and taken to the nest. First instars were mostly ignored by Myrmica sabuleti ants and they were rarely detected by Formica fusca. Older larvae were more attractive to Lasius than to the other ant genera. Pupae were very attractive to Lasius, moderately so to Myrmica, and were ignored by Formica fusca. Teneral adults were palpated by Lasius, but were attacked by Myrmica and Formica workers. We conclude that P. argus is a specialist associate of Lasius ants. Two populations of Plebejus argus were compared: one is naturally associated with Lasius niger, and the other with Lasius alienus. In reciprocal trials, larvae were slightly more attractive to their natural host ant species. Since test larvae were reared on a single host plant species in captivity, this differentiation probably has a genetic basis.     

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.     

Interspecific interference for nest sites betweenLeptothorax congruus andMonomorium intrudens

Summary Interference competition for nest sites was studied in ant communities dominated byLeptothorax congruus in the suburbs of Tokyo, central Japan. At the two study plots located in a deciduous wood and in grassland,L. congruus constructed nests in dead branches or stems of dead grasses. Approximately 50% of the nests were physically broken within a year, suggesting that they were very fragile. Of totals of 67 and 91 nests ofL. congruus marked at the two sites, 12 (17.5%) and 53 (58.2%) nests, respectively, were replaced by other ant species (Monomorium intrudens,Crematogaster brunnea teranishii,Camponotus itoi andLasius sp.) which were common in both habitats. Field observation suggested that, among these ants,M. intrudens was a major competitor usurping the nests ofL. congruus by aggressive invasion.     

Density-dependent predation of the antLasius niger (Hymenoptera: Formicidae) on two attended aphidsLachnus tropicalis andMyzocallis kuricola (Homoptera: Aphididae)

The antLasius niger was observed collecting honeydew and preying on the two aphid speciesLachnus tropicalis andMyzocallis kuricola on the chestnut treesCastanea crenata. Observation determined how the antL. niger controlled their predation on the aphids in response to the density and honeydew-productivity of the aphids.Lachnus tropicalis was a better honeydew source thanM. kuricola forL. niger in terms of the amount of honeydew collected per unit time by the ants. The number of foraging workers on a tree increased with the number ofL. tropicalis on the tree, but not with the number ofM. kuricola. The density ofL. tropicalis perL. niger worker on a tree had a positive effect on the predation activity ofL. niger on both aphids, whereas the density ofM. kuricola per ant did not have any significant effect. The predation pressure by the ant which increased withL. tropicalis density, however, directed toM. kuricola rather than toL. tropicalis. These facts suggest (1) thatL. niger control their predation activities on aphids with regards to the densities of the attended aphids per worker, and (2) that the ants prey on the aphid species producing less honeydew. The effects of the ant predation on aphids and the importance of these predation effect in antaphids interactions were discussed.     

Influence of ants (Hymenoptera: Formicidae) on honeydew excretion and escape behaviors in a myrmecophile,dalbulus quinquenotatus (Homoptera: Cicadellidae), and its congeners

Few leafhopper species are known to be ant-attended. Evidence is presented that unequivocally demonstrates that Dalbulus quinquenotatusis a myrmecophile. In a greenhouse study, the behavior of D. quinquenotatusand four Dalbulusspecies not associated with ants was observed in the absence and presence of the pavement ant, Tetramorium caespitum. D. quinquenotatusis readily contacted by tending ants and responds to stroking on the abdomen from ants' antennae by excreting and holding honeydew droplets until droplets are removed by ants. Nonattended Dalbulusspecies avoid contact with ants by walking,jumping, or flying away when approached. D. quinquenotatusexcretes three to six times the volume of honeydew as do two nonattended species, D. maidisand D. gelbus.Droplets of D. quinquenotatusare about 23% larger in diameter and excreted two to four times more frequently than for the other species. D. quinquenotatustakes about 0.15 s to form honeydew droplets on the anal tube, then holds the droplet an average of 0.28 s before expelling it when ants are absent. In the presence of ants, D. quinquenotatusholds the droplet an average of 1.31 s, which gives ants time to harvest the droplet. Nonattended species, however, immediately expel droplets from the anal tube after droplet formation. This ant-leafhopper mutualism apparently has evolved due to the ability of D. quinquenotatusto have extensive physical contact with ants and excrete large amounts of honeydew. D. chiapensis,a possible descendent of D. quinquenotatus,may secondarily have lost its mutualistic relationship with ants.     

How an ant decides to prey on or to attend aphids

The following results on the behavior decision making of the antLasius niger toward two species of myrmecophilous aphidsLachnus tropicalis andMyzocallis kuricola on chestnut trees have been found. (1) An individual worker consistently attended only one aphid species, even if her nestmates attended other aphid species on the same tree. (2) The ants preyed less on the aphid species which they attended than on other myrmecophilous aphid species. (3) The ants preyed less on the aphids which had been attended by their nestmates, even if both aphids were the same species. (4) The ants preyed less on aphids which had provided honeydew to their nestmates. (5) The increased aphid density per ant led to an increase in the rate of predation on the introduced aphids by the ants. These results suggest that each worker ofL. niger chooses aphid species to attend from her experience. In addition, the workers can recognize whether an aphid has been attended by their nestmates and whether an aphid has given their nestmates honeydew. Through these processes, each worker decides to attend or to prey on the aphid. As a result, they may realize efficient collective foraging dependent on aphid density per worker.     

Different impacts of two species of aphid-attending ants with different aggressiveness on the number of emerging adults of the aphid’s primary parasitoid and hyperparasitoids

The impacts of two species of ants (Lasius niger and Pristomyrmex pungens) attending the cotton aphid (Aphis gossypii) on the number of emerging adults of the aphids primary parasitoid (Lysiphlebus japonicus) and hyperparasitoids were assessed experimentally at a no-pesticide mandarin grove. L.japonicus females were observed foraging frequently in aphid colonies attended by either ant species, with more females in P.pungens-attended than in L.niger-attended colonies, but rarely in aphid colonies where ants were artificially excluded. Females were less often attacked by P.pungens workers than by L.niger workers, so that they stayed longer and oviposited into more aphids in P.pungens-attended than in L.niger-attended colonies. Attendance by each ant species reduced predator numbers in aphid colonies, compared to colonies where ants were absent, although P.pungens was slightly less effective in repelling predators. Therefore, both ant species incidentally protected parasitized aphids from predators. Consequently, L.japonicus-mummies were abundant in colonies attended by either ant species, with more mummies in P.pungens-attended colonies, and were scarce in ant-excluded colonies. The hyperparasitism and predation on L.japonicus larvae within mummies occurred more frequently in P.pungens-attended than in L.niger-attended colonies, but mummy predation rate was only 20% in the former. As a result, the number of emerging L.japonicus adults did not differ significantly between aphid colonies attended by the two ant species, but significantly more hyperparasitoids emerged in colonies attended by the relatively less aggressive P.pungens than in colonies attended by L.niger.     

Effects of ants on plant diversity in semi-natural grasslands

Ants (L. niger and L. flavus) build conspicuous mounds that are covered with vegetation. The aim of this study was to investigate whether the vegetation on ant mounds in semi-natural grasslands differed from that around the mounds. Another aim was to investigate whether the changes in the vegetation on ant mounds were influenced by grazing management or by habitat characteristics, semi-dry versus moist. Here, the total number of plant species and total plant cover were lower on ant mounds than in patches off-mound. The plant cover of perennials that form rosettes was twice as high on mounds inhabited by L. niger than on those inhabited by L. flavus. Only a few plant species were restricted to either ant mounds or adjacent field and the effects of ants on the plant diversity in semi-natural grasslands seemed to be low. Grazing management did not affect the differences in the vegetation on ant mounds and in equal-sized patches off-mound, whereas habitat characteristics affected ant-induced changes in vegetation cover of some plant species.