Effect of size,extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> and the hoverfly <Emphasis Type="Italic">Episyrphus balteatus</Emphasis>

Intraguild predation (IGP) is a widespread interaction between predatory arthropods, and is influenced by several factors. The harlequin ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), has frequently been reported as an intraguild predator of other Coccinellidae, but little is known about its interactions with other aphidophagous predators, including syrphids. This study investigated the incidence of IGP between H. axyridis and Episyrphus balteatus (Diptera: Syrphidae), the most abundant hoverfly species in Europe and a commercially available aphid biocontrol agent. The influence of size, presence of extraguild prey and habitat complexity were investigated through laboratory experiments in Petri dishes and on potted broad bean plants. In both types of arenas, IGP between H. axyridis and E. balteatus was found to be asymmetric, with the coccinellid in the majority of cases being the intraguild predator. There was a significant effect of size on the frequency of IGP. The efficiency of H. axyridis as an intraguild predator increased with the developmental stage. Early instars of E. balteatus were the most vulnerable to IGP. Pupae of either species were not attacked. In the presence of extraguild prey, the frequency of IGP was substantially reduced. However, IGP still occurred, mainly in combinations of older larvae of H. axyridis with first or second instars of E. balteatus. The size of the arena affected the incidence of IGP in combinations with second instars of E. balteatus, but not in combinations with third instars. Field research is needed to elucidate the ecological relevance of IGP among these predators.     

Use of selected flowering plants in greenhouses to enhance aphidophagous hoverfly populations (Diptera: Syrphidae)

The addition of floral resources in a crop is the most commonly used conservation biological control strategy. The influence of additional floral resources on the abundance of aphidophagous syrphids has been studied in Mediterranean sweet-pepper greenhouses, in southeast Spain. Sweet alyssum and coriander were the plant species used as flowering plants, distributed in the greenhouse in several monospecific patches. In our first experiment the influence on syrphid pre-imaginal stages (larvae and pupae) was studied and adult stages were studied in a second experiment. A higher number of pre-imaginal syrphids was recorded in two replicated greenhouses where flowers were introduced, compared with two control greenhouses (without additional floral resources). To evaluate the effect on adults, 4 greenhouses were divided into 2 plots in each greenhouse and flowers were introduced in one plot per greenhouse. More hoverfly adults were observed in the plots where flowers had been introduced than in the control. The three most abundant syrphid species found were Eupeodes corollae, Episyrphus balteatus and Sphaerophoria rueppellii. Specimens from these species were dissected, and their pollen content was analysed to assess the food potential of the introduced flowers. The three syrphid species fed on pollen from both the flowering plants, as well as on sweet-pepper pollen. This conservation biological control strategy is an effective method to enhance native syrphid populations in Mediterranean sweet-pepper greenhouses.     

An unusual,but not unexpected,evolutionary step taken by syrphid flies: the first record of true primary parasitoidism of ants by Microdontinae

Parasitoidism of ants by flies is known only for Phoridae and Tachinidae. We report the first record of a hoverfly (Syrphidae, Microdontinae, Hypselosyrphus) acting as a true primary parasitoid of ants. Previously, larvae of Microdontinae were known only as obligate predators of ant brood. This is also the first host record for any Hypselosyrphus species, the first reliable record of an association between a syrphid fly and a ponerine ant, and the first record of a dipteran parasitoid developing upon the immature stages of ants. We reared adults of Hypselosyrphus trigonus from cocoons of the arboreal ponerine ant, Pachycondyla villosa, nesting in Aechmea bracteata bromeliads in southern Quintana Roo, Mexico, and we succeeded in determining various aspects of the parasitoid's life history. The findings obtained in the present study provide novel insights into the evolutionary transformation and diversification of the feeding habits of microdontine syrphid larvae, from an obligatory, specific predatory association with the ant brood, to parasitoidism of ant prepupae. We also highlight the need for more detailed studies of the interactions of arboreal ants and their parasites. We conclude with an overview of the evolutionary transitions and diversification of larval feeding habits that have taken place within the family Syrphidae. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 462–472.     

The effect of egg load and host deprivation on oviposition behaviour in aphidophagous hoverflies

1. Two species of aphidophagous hoverfly, Episyrphus balteatus and Syrphus ribesii, were tested for the effects of egg load and host deprivation on oviposition choices. 2. Egg load affected the total number of eggs laid in E. balteatus but not in S. ribesii, however it did not affect the proportion laid on any one aphid in E. balteatus but did affect the proportion laid on any one aphid in S. ribesii. The rank order of preferences remained unchanged by age or host deprivation. 3. The dominant effects on host choices were aphid species (in both syrphids) and presentation order (in E. balteatus). 4. Being deprived of hosts increased egg load substantially in E. balteatus, and increasing time of deprivation also had an effect on discrimination; there was no effect of host deprivation in S. ribesii. 5. Reasons for these patterns are discussed.     

Assessment of aphid colonies by hoverflies. II pea aphids and 3 syrphid species;Betasyrphus serarius (Wiedemann),Metasyrphus frequens Matsumura andSyrphus vitripennis (Meigen) (Diptera: Syrphidae)

In the aphidophagous syrphid species,Betasyrphus serarius (Wiedemann),Metasyrphus frequens Matsumura andSyrphus vitripennis (Meigen), females in search of oviposition sites assess the qualitative and quantitative value of pea aphid colonies for securing the successful development of their offspring. They select, as their oviposition sites, young and “promising” aphid colonies consisting of nymphs and/or adult aphids including few winged adults. They neglect large, older colonies of 4th-instar nymphs and/or winged adult aphids. The 3 syrphid species adopt “buy-futures” ovipositional tactic as doesEpisyrphus balteatus (de Geer), although some tinge of “spot-transaction” is noticed inM. frequens andS. vitripennis.     

The function of extrafloral nectaries in the pollination and reproduction of Sambucus javanica

Sambucus javanica is a perennial herb with extrafloral nectaries (EFNs) on its inflorescences. To explore the ecological functions of EFNs, a factorial combination experiment of ant (access or exclusion) and EFNs (with or without) at the plant level was created in two populations. The role of EFNs in the attraction of ants and flying pollinators, the defensive role of ants against foliar herbivores, the effects of ants on pollinator visitation and the effects of ant–pollinator interactions on fruit production in one or both populations were assessed. Ants were common on the ant-access plants with EFNs, but absent from the ant-access plants without EFNs. Foliar herbivory was independent of ant and EFN treatments and their interactions. The visitation frequency of flying pollinators (honeybees and syrphid flies) and fruit set were significantly higher for plants with EFNs than plants without EFNs, but were not affected by ant treatments or their interactions with EFN treatments. These results suggest that EFNs in S. javanica attracted both ants and flying pollinators, but ants did not present a defensive role against herbivores, did not deter flying pollinators from visiting inflorescences and had no effects on fruit production. In addition, ants were not significant pollen vectors.     

Some host-plant factors affecting oviposition by aphidophagous Syrphidae (Diptera)

Although most aphidophagous syrphid species lay their eggs close to aphids, Platycheirus peltatus (Meig.), Melanostoma scalare (F.) and M. mellinum (L.) laid freely on uninfested brussels sprout plants. The existence of species that will lay in the absence of aphids may be valuable in biological control and also provides a useful tool for the investigation of non-aphid oviposition stimuli. Plant species and plant appearance were both important factors in P. peltatus oviposition. Particular sites on the plant were chosen for oviposition by Syrphus balteatus (Deg.). The nature of the substrate at the oviposition site affected the size of the egg batches laid there by M. scalare, M. mellinum, P. peltatus and P. clypeatus (Meig.). The possibility is discussed that plant-location is the older-established system of host-finding and that an aphid-location system has gradually superseded it during the evolution of the obligatorily aphidophagous Syrphinae.     

Assessment of aphid colonies by hoverflies. III Pea aphids andEpisyrphus balteatus (de Geer) (Diptera: Syrphidae)

The syrphid flyEpisyrphus balteatus (de Geer) migrating from maple trees to leguminous plants in mid-April, assesses the qualitative and quantitative value of pea aphid colonies for securing successful development of her offspring. She selects young and “promising” pea aphid colonies of small size. This generally agrees with the “buy-futures” ovipositional tactic the syrphid fly adopts when it utilizes the maple aphids. The advantage of a “buy-futures” ovipositional tactic found in many syrphid species is discussed in comparison with other aphidophagous insects.     

Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management

Trichome-based tomato resistance offers the potential to reduce pesticide use, but its compatibility with biological control remains poorly understood. We evaluated Episyrphus balteatus De Geer (Diptera, Syrphidae), an efficient aphidophagous predator, as a potential biological control agent of Myzus persicae Sulzer (Hemiptera, Aphididae) on trichome-bearing tomato cultivars. Episyrphus balteatus’ foraging and oviposition behavior, as well as larval mobility and aphid accessibility, were compared between two tomato cultivars (Lycopersicon esculentum Mill. ‘Moneymaker’ and ‘Roma’) and two other crop plants; broad bean (Vicia faba L.) and potato (Solanum tuberosum L.). Hoverfly adults landed and laid more eggs on broad beans than on three species of Solanaceae. Hoverfly larval movement was drastically reduced on tomato, and a high proportion of hoverfly larvae fell from the plant before reaching aphid prey. After quantifying trichome abundance on each of these four plants, we suggest that proprieties of the plant surface, specifically trichomes, are a key factor contributing to reduced efficacy of E. balteatus as a biological agent for aphid control on tomatoes. Handling editor: Stanislaw Gorb     

Stable isotope investigation of a cryptic ant-plant association: Myrmelachista flavocotea (Hymenoptera, Formicidae) and Ocotea spp. (Lauraceae)

An obligate symbiosis between Ocotea dendrodaphne Mez and O. atirrensis Mez & Donn.Sm. (Lauraceae) and their cryptic ant symbiont, Myrmelachista flavocotea, is common in lowland wet forests of Costa Rica, yet it is unclear whether the association is typically mutualistic or parasitic. Ants impose costs by tending trophobionts inside the plant body and further compromise the structural integrity of their host by hollowing its stems. Benefits to the host, including anti-herbivore defense and nutrient provisioning, must outweigh these costs for the association to be mutualistic, but benefits in this system are largely unknown. We adopted a stable isotope approach to investigate trophic relationships among Ocotea hosts, coccoid trophobionts, and worker and larval ants in the understory of mature forest at La Selva Biological Station, Costa Rica. In addition, a natural stable isotope marker (tuna) was made available to M. flavocotea colonies to determine whether ants are fortuitous scavengers and/or provision their host. In this system, we found unusual patterns of isotopic fractionation. For coccoids, nitrogen isotopes are only slightly enriched, and carbon isotopes were depleted relative to the host signature. Moreover, nitrogen signatures of the timid Myrmelachista ants are high, suggesting a substantial degree of carnivory and/or scavenging in this species. In the provisioning study, ant colonies provided with baits demonstrated a significant shift in carbon isotopic composition relative to untreated colonies indicating uptake and assimilation of the bait. These results suggest that these timid ants are patrolling the plant for food and concentrating nutrients in Ocotea’s hollowed stems. Further studies are required to confirm if M. flavocotea provides a net benefit to its host by providing nutrients, reducing herbivory, or by removing detrimental debris from the plants surface.     

Assessment of the maple aphid colony by the hover fly,Episyrphus balteatus (de Geer) (Diptera: Syrphidae) I

The aphidophagous syrphid fly,Episyrphus balteatus (de Geer), actively visits the Japanese maple,Acer palmatum Thunb., in early spring and oviposits adjacent to colonies of 2 maple aphids,Periphyllus californiensis (Shinji) andYamatocallis tokyoensis (Takahashi). Female flies, in the field, chose small, young colonies with nymphs and wingless adult aphids for their oviposition sites rather than older colonies including winged adults. Same tendency was clearly observed in the experiments with models. It was demonstrated experimentally that they can discriminate between the wingless and winged adult models. It is suggested that females of the hover fly assess the value of aphid colonies as the food resource of their offspring. Contribution No. 211 from Lab. Entomol., Kyoto Pref. Univ.     

Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity

We studied the association between the honeydew-producing membracid Guayaquila xiphias and its tending ants in the cerrado savanna of Brazil, during 1992 and 1993. Results showed that ants attack potential enemies of G. xiphias, and that increased ant density near the treehoppers affects the spatial distribution of parasitoid wasps on the host plant, keeping them away from brood-guarding G. xiphias females. Controlled ant-exclusion experiments revealed that ant presence (seven species) reduces the abundance of G. xiphias’ natural enemies (salticid spiders, syrphid flies, and parasitoid wasps) on the host plant. The data further showed that ant-tending not only increased homopteran survival, but also conferred a direct reproductive benefit to G. xiphias females, which may abandon the first brood to ants and lay an additional clutch next to the original brood. Two years of experimental manipulations, however, showed that the degree of protection conferred by tending ants varies yearly, and that at initially high abundance of natural enemies the ant species differ in their effects on treehopper survival. Ant effects on treehopper fecundity also varied with time, and with shifts in the abundance of natural enemies. This is the first study to simultaneously demonstrate conditionality in ant-derived benefits related to both protection and fecundity in an ant-tended Membracidae, and the first to show the combined action of these effects in the same system. Received: 19 October 1999 / Accepted: 14 February 2000     

Larval interactions in aphidophagous predators: effectiveness of wax cover as defence shield of Scymnus larvae against predation from syrphids

Small-sized predators in the aphidophagous guild of Aphis gossypii Glover colonies on hibiscus trees in Japan exploit aphids at low prey abundance. Scymnus (Pullus) posticalis Sicard beetles were the first predatory species to attack aphids in the spring, and their larvae co-occurred with larvae of Eupeodes freguens (Matsumura) syrphids in aphid-infested leaves of hibiscus for 3 weeks in absence of large-sized coccinellid predators. Larval interaction between Scymnus and syrphid predators was examined in relation to effectiveness of wax cover of Scymnus against predation from syrphids. Waxless first instar larvae were not protected but wax-covered larvae of second, third and fourth instars were protected from predation by syrphid larvae. The protection was lower in the second instar which has a thin wax cover and significantly higher in the third and fourth instars having a thick wax cover. In addition, larvae from which the wax was removed were significantly more vulnerable to predation. Vulnerability of Scymnus larvae to predation from syrphids was directly related to the thickness of wax cover. Results suggest that the wax cover of Scymnus larvae act as an effective defence mechanism against predation from syrphid larvae.     

Effect of stinging nettle habitats on aphidophagous predators and parasitoids in wheat and green pea fields with special attention to the invader Harmonia axyridis Pallas (Coleoptera: Coccinellidae)

The relative occurrence and seasonal abundance of aphids and their natural enemies were visually assessed between May and July 2005–2006 in four types of habitats located in Gembloux (Namur province, Belgium): green pea, wheat and stinging nettle either planted in or naturally growing in woodland adjacent to these crops. Results showed that: (i) Acyrthosiphon pisum Harris, Sitobion avenae F. and Microlophium carnosum Buckton were the most common aphid species, respectively, on green pea, wheat and stinging nettle either in or near field crops; (ii) stinging nettle and field crops shared several important aphidophagous insect species such as the ladybird Coccinella septempunctata L., hoverfly Episyrphus balteatus De Geer and braconid wasp Aphidius ervi Haliday; (iii) the shared beneficial species were typically recorded earlier on stinging nettles than on crops; and (iv) the spatial occurrence of the invasive ladybird Harmonia axyridis Pallas was distinctly associated with stinging nettles, particularly in 2005. Stinging nettles and field crops partially coincide in time, enabling the movement of natural enemies among them. These findings suggest that the presence of stinging nettles in landscapes seems to enhance the local density of aphidophagous insect communities necessary for aphid biocontrol in field crops.     

Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards

Abstract 1. The Argentine ant, Linepithema humile, tends honeydew‐excreting homopterans and can disrupt the activity of their natural enemies. This mutualism is often cited for increases in homopteran densities; however, the ant’s impact on natural enemies may be only one of several effects of ant tending that alters insect densities. To test for the variable impacts of ants, mealybug and natural enemy densities were monitored on ant‐tended and ant‐excluded vines in two California vineyard regions. 2. Ant tending increased densities of the obscure mealybug, Pseudococcus viburni, and lowered densities of its encyrtid parasitoids Pseudaphycus flavidulus and Leptomastix epona. Differences in parasitoid recovery rates suggest that P. flavidulus was better able to forage on ant‐tended vines than L. epona. 3. Densities of a coccinellid predator, Cryptolaemus montrouzieri, were higher on ant‐tended vines, where there were more mealybugs. Together with behavioural observations, the results showed that this predator can forage in patches of ant‐tended mealybugs, and that it effectively mimics mealybugs to avoid disturbance by ants. 4. Ant tending increased densities of the grape mealybug, Pseudococcus maritimus, by increasing the number of surviving first‐instar mealybugs. Parasitoids were nearly absent from the vineyard infested with P. maritimus. Therefore, ants improved either mealybug habitat or fitness. 5. There was no difference in mealybug distribution or seasonal development patterns on ant‐tended and ant‐excluded vines, indicating that ants did not move mealybugs to better feeding locations or create a spatial refuge from natural enemies. 6. Results showed that while Argentine ants were clearly associated with increased mealybug densities, it is not a simple matter of disrupting natural enemies. Instead, ant tending includes benefits independent of the effect on natural enemies. Moreover, the effects on different natural enemy species varied, as some species thrive in the presence of ants.     

Convergence of chemical mimicry in a guild of aphid predators

Abstract.  1. A variety of insects prey on honeydew-producing Homoptera and many do so even in the presence of ants that tend, and endeavour to protect, these trophobionts from natural enemies. Few studies have explored the semiochemical mechanisms by which these predators circumvent attack by otherwise aggressive ants.
2. Ants use specific mixtures of cuticular hydrocarbons (CHCs) as recognition labels, but this simple mechanism is frequently circumvented by nest parasites that engage in 'chemical mimicry' of their host ants by producing or acquiring a critical suite of these CHCs.
3. Analysis of the CHCs from the North American woolly alder aphid, Prociphilus tessellatus (Homoptera: Aphididae), their tending ants, and aphid predators from three insect orders, Feniseca tarquinius (Lepidoptera: Lycaenidae), Chrysopa slossonae (Neuroptera: Chrysopidae), and Syrphus ribesii (Diptera: Syrphidae), showed that while the CHC profile of each predatory species was distinct, each was chemically more similar to the aphids than to either tending ant species. Further, the CHCs of each predator species were a subset of the compounds found in the aphids' profile.
4. These results implicate CHCs as a recognition cue used by ants to discriminate trophobionts from potential prey and a probable mechanism by which trophobiont predators circumvent detection by aphids and their tending ants.
5. Although several features of the aphids' CHC profile are shared among the chemically mimetic taxa, variation in the precision of mimicry among the members of this predatory guild demonstrates that a chemical mimic need not replicate every feature of its model.     

Dealing with food shortage: larval dispersal behaviour and survival on non‐prey food of the hoverfly Episyrphus balteatus

1. Predatory larvae often have to face food shortages during their development, and thus the ability to disperse and find new feeding sites is crucial for survival. However, the dispersal capacity of predatory larvae, the host finding cues employed, and their use of alternative food sources are largely unknown. These aspects of the foraging behaviour of the aphidophagous hoverfly (Episyrphus balteatus De Geer) larvae were investigated in the present study. 2. It was shown that these hoverfly larvae do not leave a plant as long as there are aphids available, but that dispersing larvae are able to find other aphid colonies in the field. Dispersing hoverfly larvae accumulated on large aphid colonies, but did not distinguish between different pea aphid race–plant species combinations. Large aphid colonies might be easier to detect because of intensified searching by hoverfly larvae following the encounter of aphid cues like honeydew that accumulate around large colonies. 3. It was further shown that non‐prey food, such as diluted honey or pollen, was insufficient for hoverfly larvae to gain weight, but prolonged the survival of the larvae compared with unfed individuals. As soon as larvae were switched back to an aphid diet, they rapidly gained weight and some pupated after a few days. Although pupation and adult hatching rates were strongly reduced compared with hoverflies continuously fed with aphids, the consumption of non‐prey food most probably increases the probability that hoverfly larvae find an aphid colony and complete their development.     

Predatory hoverflies select their oviposition site according to aphid host plant and aphid species

The hoverfly Episyrphus balteatus De Geer (Diptera: Syrphidae) is an abundant and efficient aphid‐specific predator. Several aphidophagous parasitoids and predators are known to respond positively to aphid‐infested plants. Semiochemicals from the latter association usually mediate predator/parasitoid foraging behavior toward sites appropriate for offspring fitness. In this study, we investigated the effect of aphid host plant and aphid species on foraging and oviposition behavior of E. balteatus. Behavioral observations were conducted using the Noldus Observer v. 5.0, which allows observed insect behavior to be subdivided into different stages. Additionally, the influence of aphid species and aphid host plant on offspring fitness was tested in a second set of experiments. Acyrthosiphon pisum Harris and Megoura viciae Buckton were equally attractive for E. balteatus whereas Aphis fabae Scopoli (all Homoptera: Aphididae) were less attractive. These results were correlated with (i) the number of eggs laid, which was significantly higher for the two first aphid species, and (ii) the fitness of hoverfly larvae, pupae, and adults. Two solanaceous plant species, Solanum nigrum L. and Solanum tuberosum L. (Solanaceae), which were infested with Myzus persicae Sulzer (Homoptera: Aphididae), were also compared using the same approach. Discrimination between these two M. persicae host plants was observed, with S. tuberosum being preferred as an oviposition site by the predatory hoverfly. Larval and adult fitness was correlated with the behavioral observations. Our results demonstrated the importance of the prey–host plant association on the choice of the oviposition site by an aphid predator, which is here shown to be related to offspring fitness.     

Fenologia y seleccion de habitat de las especies de sirfidos afidofagos (Dipt.: Syrphidae) mas frecuentes en cultivos cerealeros y forrajeros en la provincia de buenos aires,argentina

Phenology and habitat selection of the aphidophagous syrphid species most frequently found in crops and pastures in the Province of Buenos Aires, Argentina. The paucity in ecological studies on aphidophagous syrphid flies (Diptera, Syrphidae) of the neotropical region is particularly pronounced in Argentina. In order to increase the database on these natural enemies, the phenology and habitat selection of six syrphid flies (Dipt., Syrphidae):Syrphus phaeostigma (L.);Allograpta obliqua (Wied.);Allograpta exotica (Wied.);Pseudodorus clavatus (L.);Platycheirus carposcalis (L.) andOcyptamus argentinensis (Thorn.) were studied in the Province of Buenos Aires (Argentina). The moment of the year in which adults, eggs, larvae and pupae of these species are found was recorded. The phenologies found for the species in our area are similar to those found for other species of the same genera in other parts of the world. These aphidophagous syrphids are not evenly distributed in all the systems sampled, evidencing a preference for either one of the following types of habitat: cereal crop, lucerne, soya, bushes or prairies. These results are potentially useful in terms of crop and pest management practices.