Host-range study about four aphid parasitoid species among 16 aphid species for constructing banker–plant systems

To provide fundamental information for the biological control of aphids in vegetable greenhouses, we compared the host ranges of four aphid parasitoid species, Aphidius colemani Viereck, Aphidius gifuensis Ashmead, Diaeretiella rapae (M’Intosh), and Ephedrus nacheri Quilis (Hymenoptera: Braconidae: Aphidiinae). The acceptability as host of 11 vegetable-pest aphids, Acyrthosiphon pisum (Harris), Aphis craccivora Koch, Aphis gossypii Glover, Aulacorthum solani (Kaltenbach), Brevicoryne brassicae (Linnaeus), Chaetosiphon fragaefolii (Cockerell), Lipaphis erysimi (Kaltenbach), Macrosiphoniella sanborni (Gillette), Macrosiphum euphorbiae (Thomas), Myzus persicae (Sulzer), and Uroleucon formosanum (Takahashi), in addition to five aphid species, Melanaphis sacchari (Zehntner), Rhopalosiphum maidis (Fitch), Rhopalosiphum padi (Linnaeus), Schizaphis graminum (Rondani), and Sitobion akebiae (Shinji) (Hemiptera: Aphididae) that serve as alternative hosts in banker–plant systems for the four aphid parasitoid species, were investigated. A newly emerged pair of parasitoid adults were provided to 100 aphids of each species on caged host plants in a 25 °C chamber for 24 h. The numbers of mummified aphids and emerged adults were counted in 10 trials for each aphid species. Aphidius colemani, A. gifuensis, D. rapae and E. nacheri parasitized four, two, three, and eight pest species, respectively, and four, three, three, and five alternative host species, respectively. Ephedrus nacheri had the broadest host range among the four species, and all the four species parasitized M. persicae, R. maidis, and S. graminum. This information will be useful for selecting candidate of biological control agents for aphids and for constructing banker–plant systems.

     

Indirect interactions in aphid–parasitoid communities

Indirect interactions between populations of different species can be important in structuring natural communities. Indirect effects are either mediated by changes in population densities (trophic or density-mediated effects) or by changes in the behavior of species that are not trophically connected (behavioral or trait-mediated effects). We reviewed the literature on aphids and their parasitoids to explore the various possible indirect interactions that can occur in such communities. The review was motivated by our study of a particular aphid–parasitoid community in a natural (i.e., nonagricultural) habitat, and by the wealth of information that exists about aphid–parasitoid systems in agricultural settings. We focused our review on aphid–parasitoid interactions, but considered how these were influenced by the other aphid natural enemies and also by aphid mutualists and host plants. We conclude that indirect effects are likely to have a major effect in structuring aphid–parasitoid communities, and that the latter are a valuable model system for testing ideas about community interactions. Received: December 20, 1998 / Accepted: January 12, 1999     

Plant–rhizobia interactions alter aphid honeydew composition

Both above- and below-ground interspecific interactions contribute to ecosystem functioning in terrestrial systems, and the integration of below- and above-ground interactions is crucial for deepening our knowledge of nutrient cycling and community dynamics in terrestrial ecosystems. The present study explored the effects of plant–microbe interactions on aphid honeydew quality and quantity and important factors mediating ant–aphid mutualisms and below-ground nutrient dynamics. Soybean aphids (Aphis glycines) were inoculated onto two closely related strains of soybean plants: a nodulating strain that associates with rhizobia and a non-nodulating strain that does not harbor any nitrogen-fixing bacteria. As expected, prior to aphid inoculation, nodulating plants were significantly taller and had more leaves than non-nodulating plants. Aphids feeding on nodulating strains were found to reach slightly larger colony sizes and produce honeydew with significantly different sugar profiles than those feeding on non-nodulating plants. The honeydew collected from aphid colonies feeding on nodulating plants contained 160 % more total sugars than honeydew collected from colonies feeding on non-nodulating plants, but there was no difference in total amino acid-N content in honeydew from colonies feeding on the different plant strains. We discuss the implications of honeydew composition for nutrient cycling and community dynamics and suggest areas of future research to elucidate the consequences of altered aphid honeydew composition on ecosystem properties.     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Defensive ant,aphid and caterpillar mimicry in plants?

Here we describe three apparently novel types of visual insect mimicry in plants. In the first type, plants of Xanthium trumarium L. have dark spots and flecks that resemble ants (Formicidae) in size and shape in the epidermis of stems, branches and petioles, and plants of Arisarum vulgare Targ.-Tozz. have them on petioles and inflorescence stems. In the second type, the dark anthers of Paspalum paspaloides (Michaux) Scribner (= P. distichum ) are the size, shape and colour of aphids (Homoptera; Aphidoidea) and they sway in the wind like swivelling aphids. Similarly, the stems of Alcea setosa (Boiss.) Alef. are covered with dark flecks that look like aphids. Finally, immature pods of three wild annual legumes ( Lathyrus ochrus (L.) DC.; Pisum fulvum Sm.; Vicia peregrina L.) have conspicuous reddish spots, arranged along the pods, that appears to mimic lepidopteran caterpillars. In one of the species ( V . peregrina ) two different mimicking morphs were found. We propose that these morphological traits may serve as herbivore repellent cues and are part of the defence system of the plants.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 393–398.     

How many soldiers are optimal for an aphid colony?

A number of aphid species produce sterile soldiers that defend their colony-mates against predators. How many soldiers should a colony produce? Assuming logistic growth of the aphid colony, we can theoretically deduce that soldiers will be produced until the marginal defensive efficacy of a soldier diminishes to rm/K, a ratio of two exogenous variables of the logistic equation, which are the maximum intrinsic rate of increase and carrying capacity. This conclusion holds true irrespective of the number of founders. As the number of founders increases, the entire colony size becomes larger, thus decreasing the percentage of soldiers. In case of multiple founders, each clone will produce the same number of reproductives that remain on the hostplant.     

How does the host-specialized aphid deal with food deficiency？

Aphis gossypii Glover shows obvious host specialization, with cucurbit- and cotton-specialized biotypes or host races in many regions. Because its annual natal hostcrops senesce earlier the cucurbit-specialized biotype may suffer food deficiency. The method this biotype uses to overcome this challenge is still poorly understood. In orderto understand the potential of the cucurbit-specialized biotype aphids in host shift and usage, the performance of this biotype on cotton （Gossypium hirsutum）, a common butpoor quality host plant, was explored in this study. The cucurbit-specialized aphids could establish populations on cotton only when these plants had at least nine leaves, and subsequent populations developed rather slowly. The presence of whitefly populations on cotton improved the success rate of cucurbit-specialized aphids. The cucurbit-specialized aphidswere mainly distributed on the older leaves of cotton, with only a few settling on the upper leaves. The cucurbit-specialized aphids reared on cotton for 40, 54 and 61 days stillmaintained strong preference for their natal host plant, cucumber （Cucumis sativus）, rather than cotton, and their net reproductive rates and intrinsic rates of natural increase weredramatically lower when they were transferred onto new six-leaf cotton plants or detached leaves. Therefore, we concluded that the cucurbit-specialized aphids have the potentialto utilize mature or whitefly-stressed cotton plants, but that this feeding experience on cotton did not alter their specialization for cucurbits. Some cotton plants could act as atemporary host for the cucurbit-specialized aphids to overcome food deficiency arising from senescing cucurbits.     

Melatonin in the seasonal response of the aphid Acyrthosiphon pisum

Aphids display life cycles largely determined by the photoperiod.During the warm long-day seasons.most aphid species reproduce by viviparous parthenogenesis.The shortening of the photoperiod in autumn induces a switch to sexual reproduction.Males and sexual females mate to produce overwintering resistant eggs.In addition to this full life cycle(holocycle),there are anholocyelic lineages that do not respond to changes in photoperiod and reproduce continuously by parthenogenesis.The molecular or hormonal events that trigger the scasonal response(i.c,induction of the sexual phenotypes)are still unknown.Although circadian synthesis of melatonin is known to play a key role in vertebrate photoperiodism,the involvement of the circadian clock and/or of the hor-mone melatonin in insect seasonal responses is not so well established.Here we show that melatonin levels in the aphid Acyrthosiphon pisum are significantly higher in holocyclice aphids reared under short days than under long days,while no differences were found between anholoeyelic aphids under the same conditions.We also found that melatonin is localized in the aphid suboesophageal ganglion(SOG)and in the thoracic ganglionic mass(TGM).In analogy to vertcbrates,insect-type arylalkxylamine N-acetyltransferases(i-AANATs)are thought to play a key role in melatonin synthesis.We measured the expression of four I-AANAT genes identified in A.pisum and localized two of them in situ in the insect central nervous systems(CNS).Levels of expression of these genes were compatible with the quantities of melatonin observed.Moreover,like melatonin,expression of these genes was found in the SOG and the TGM.     

Phenol oxidising enzymes in the grain aphid’s saliva

Sucrose-agarose gels and sucrose liquid diets were used to study the phenol oxidising enzymes in the salivary secretions of the grain aphid, Sitobion avenae (Fabricius). Activity indicating the presence of two oxidoreductases, polyphenol oxidase (PPO) and peroxidase (Px), was found. Both enzymes were present in the aphids stylet sheath (gelling saliva) but only polyphenol oxidase activity was found in the halos around sheaths and thus in watery saliva. Electrical penetration graphs (EPG) revealed that the secretion of these enzymes into the gels, by an individual aphid, was associated with its probing activity observed during penetration of the epidermal and mesophyll tissues. The grain aphids PPO, secreted in its saliva reacted with a range of phenolic compounds. As most of these phenolics occur naturally in cereals, the grain aphid could modify its host-plants phenolic composition. The importance of the grain aphids polyphenol oxidase and peroxidase in detoxifying cereal phenolics is discussed.     

Scaling up population dynamic processes in a ladybird–aphid system

Here, we study how scaling up to the metapopulation level affects predictions of a population dynamics model motivated by an aphidophagous predator–aphid system. The model incorporates optimization of egg distribution in predatory females, cannibalism among their offspring, and self-regulation of the prey population. These factors determine the within-year dynamics of the system and translate the numbers of prey and predator individuals at the beginning of the season into their numbers at the end of the season at the level of one patch—one suitable host plant or a group of these. At the end of each season, all populations of prey and all populations of predators are mixed (this simulates aphid host-alternation and ladybird migration to hibernation sites), and then redistributed at the beginning of the next season. Prey individuals are distributed at random among the patches as a “prey rain”, while adult predators that survived from the previous season optimize the distribution of their offspring, in that they prefer patches with sufficient amount of prey and absence of other predators. This redistribution followed by within-season dynamics is then iterated over many seasons. We look at whether small-scale trends in population dynamics predicted by this model are consistent with large-scale outcomes. Specifically, we show that even on the metapopulation scale, the impact of predators on prey metapopulation is relatively low. We further show how the dates of predator arrival to and departure from the system affect the qualitative behaviour of the model predictions.     

Impact of a gall-inducing aphid on Pistacia atlantica Desf. trees

The impact of gall-inducing aphids on shoot development was analyzed in 900 shoots from 20 pistachio trees, Pistacia atlantica Desf. (Anacardiaceae): 600 in which the axillary—lateral buds were galled by Slavum wertheimae HRL during the previous growth season, and 300 ungalled shoots. Although P. atlantica is a compensating tree, and the aphids do not attack the apical buds, further development of shoots from the apical buds was stopped in 62% of the galled shoots, while only 8.7% of nongalled shoots stopped their growth. Further development was stopped more often on shoots carrying two or more galls than on shoots supporting only one gall. To assess the hypothesis that bud destruction by the aphids explains this pattern, a field experiment was conducted in 140 shoots, distributed across seven trees. One, two or three axillary buds from five shoots of each tree were removed for each treatment, and five other shoots were marked as controls. Only 14 shoots (10%) of the 140 did not develop. The growth of the other shoots was not very different among the treatments. The colonization of the apical shoots, which developed on previously treated shoots, by three other galling aphid species was monitored. Removing lateral buds considerably reduced the establishment of Geoica sp. galls (70% of them colonized control shoots), but weakly influenced Forda riccobonii (Stefani). It also contributed only 5% of the total variance of the distribution of Smynthurodes betae West. The different results of the survey and the experiment show that the impact of S. wertheimae galls on the future growth of shoots from apical buds is more complex than the simple physical destruction of the axillary buds. Handling editor: Graham Stone     

Estimating ancestral geographical distributions: a Gondwanan origin for aphid parasitoids?

We tested the published hypothesis of a Gondwanan origin for the overwhelmingly northern hemisphere aphid parasitoids (Aphidiinae) as follows: (i) finding their sister group by a phylogenetic analysis of the entire Braconidae (Insecta: Hymenopterai using sequence data from approximately 500 bp fragments of both the nuclear 28S (D2 region) and mitochondrial 16S rDNA genes, (ii) using this sister-group relationship and the more informative 28S D2 gene to estimate the phylogeny of the Aphidiinae and (iii) estimating the ancestral distribution for the Aphidiinae using maximum-likelihood and maximum-parsimony methods. Both methods indicated a Gondwanan origin.     

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.     

How does the host‐specialized aphid deal with food deficiency?

Aphis gossypii Glover shows obvious host specialization, with cucurbit‐ and cotton‐specialized biotypes or host races in many regions. Because its annual natal host crops senesce earlier the cucurbit‐specialized biotype may suffer food deficiency. The method this biotype uses to overcome this challenge is still poorly understood. In order to understand the potential of the cucurbit‐specialized biotype aphids in host shift and usage, the performance of this biotype on cotton (Gossypium hirsutum), a common but poor quality host plant, was explored in this study. The cucurbit‐specialized aphids could establish populations on cotton only when these plants had at least nine leaves, and subsequent populations developed rather slowly. The presence of whitefly populations on cotton improved the success rate of cucurbit‐specialized aphids. The cucurbit‐specialized aphids were mainly distributed on the older leaves of cotton, with only a few settling on the upper leaves. The cucurbit‐specialized aphids reared on cotton for 40, 54 and 61 days still maintained strong preference for their natal host plant, cucumber (Cucumis sativus), rather than cotton, and their net reproductive rates and intrinsic rates of natural increase were dramatically lower when they were transferred onto new six‐leaf cotton plants or detached leaves. Therefore, we concluded that the cucurbit‐specialized aphids have the potential to utilize mature or whitefly‐stressed cotton plants, but that this feeding experience on cotton did not alter their specialization for cucurbits. Some cotton plants could act as a temporary host for the cucurbit‐specialized aphids to overcome food deficiency arising from senescing cucurbits.     

New data on aphid fauna (Hemiptera,Aphididae) in?Algeria

A survey of aphids was carried out during the period 2008-2011 in different regions of Algeria by collecting and identifying aphids and their host plants. Aphids were collected from 46 host plants. Forty-six species were reported including thirty-six species which were recorded for the first time in this country and thirty species which were recorded for the first time in the Maghreb (North Africa). This study extends the number of known Algerian aphid to 156 species.     

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.     

The involvement of peroxidases in soybean seedlings’ defense against infestation of cowpea aphid

Changes in the level of hydrogen peroxide (H₂O₂) and activity of peroxidases towards phenolic substrates (EC 1.11.1.7) such as pyrogallol (PPX), syringaldazine (SPX) and guaiacol (GPX), and cytosolic ascorbate peroxidase (cAPX, EC 1.11.1.11) in response to infestation of cowpea aphid (Aphis craccivora Koch) were analyzed in soybean (Glycine max (L.) Merr. cv. “Nam Dan”) at the V3 stage (first two trifoliate leaves fully developed, third trifoliate leaf unrolled) for 96 h post-infestation (hpi). Influence of A. craccivora at a varied population size (10, 20 and 30 individuals per each soybean plant) caused a burst of H₂O₂ generation in the aphid-infested leaves at 12 hpi. Paralleling the H₂O₂ accumulation, peroxidase activity in all the infested plants remarkably increased and was significantly higher than that observed in controls (uninfested plants). The cascade of enzymes induced was continuously overlapped by the early enhancement of SPX within 6–24 hpi, an expression of cAPX (12–48 hpi) followed by an accumulation of GPX (24–72 hpi) and PPX (24–96 hpi). The differential induction of SPX, GPX, PPX and cAPX resulted in a rapid reduction of H₂O₂ content in aphid-infested leaves, and the activity of peroxidase was closely correlated with the intensity of A. craccivora infestation around the defined points of time at which the activity of each enzyme reached the maximum level. The increase in activity of peroxidases matched their function as controlling accumulation of H₂O₂ and detoxifying this reactive oxygen product when soybean plants were challenged with cowpea aphid. Furthermore, peroxidases could directly deter cowpea aphid feeding through other functions such as the anti-nutritive and/or toxicological defenses and/or limiting the penetration of aphid stylets into plant tissues via participating to strengthen and reinforce the cell wall barrier. These results indicated that peroxidases may be some elements of the defense system that increased the resistance of G. max cv. “Nam Dan” to infestation of A. craccivora.     

Do ecological niches differ between sexual and asexual lineages of an aphid species?

According to environmental-based theories on the maintenance of sexual reproduction, sexual and asexual populations may coexist if they occupy different ecological niches. The aphid Rhopalosiphum padi offers a good opportunity to test this hypothesis since sexual and asexual lineages show local coexistence during a large part of their respective life-cycles. Because these two reproductive variants are morphologically identical but genetically distinct, we first characterized them using genetic markers in populations of R. padi in areas where sexual and asexual lineages may occur in sympatry. We then inferred the natal host plant of sexual and asexual genotypes by analysing stable isotopic ratios and showed that sexual ones mostly originated from C₃ Poaceae while asexual ones originated from C₃ and C₄ plants, although the majority came from C₄ Poaceae. These findings indicate that ecological niches of sexual and asexual lineages of R. padi differ, offering a plausible explanation for the local coexistence of the two reproductive modes in this species through habitat specialisation.     

Farming practices change food web structures in cereal aphid–parasitoid–hyperparasitoid communities

Agricultural intensification has been shown to result in a decline in biodiversity across many taxa, but the changes in community structure and species interactions remain little understood. We have analysed and compared the structure of feeding interactions for cereal aphids and their primary and secondary parasitoids in organically and conventionally managed winter wheat fields using quantitative food web metrics (interaction evenness, generality, vulnerability, link density). Despite little variation in the richness of each trophic group, food web structures between the two farming systems differed remarkably. In contrast to common expectations, aphids and primary parasitoids were characterized by (1) a higher evenness of interaction frequencies (interaction evenness) in conventional fields, which cascaded to interactions at the next trophic level, with (2) a higher interaction evenness, (3) a higher ratio of primary parasitoid taxa per secondary parasitoid (generality) and (4) a higher link density. Aphid communities in the organically managed fields almost exclusively consisted of a single ear-colonizing species, Sitobion avenae, while highly fertilized conventional fields were mainly infested by leaf-colonizing aphids that benefit from the nutritional status of winter wheat. In conclusion, agricultural intensification appears to foster the complexity of aphid–parasitoid food webs, thereby not supporting the general expectation on the importance of organic farming practices for species richness and food web complexity.