Effect of flower identity and diversity on reducing aphid populations via natural enemy communities

Floral plantings are often used in agriculture to attract pollinator communities, but they also play an important role in recruiting and establishing natural communities for natural pest control. Inconsistent effects of floral plantings for pest control may be a result of an absence of mechanistic insights and a reliance on the idea that simply increasing flower diversity will benefit these services. A more tailored set of flower species may be needed to benefit the natural enemies through provision of nectar and alternative prey. We used an outside pot experiment to investigate the effect of three flower plants (Fagopyrum esculentum, Vicia faba, and Trifolium pratense) on reducing aphid pests on four different plant cultivars of barley (Hordeum vulgare), over two years. We grew the four cultivars of barley alone, next to a single flower or next to a mixture of flowers, and observed aphid and natural enemy colonization across the growing season. Aphid population sizes were reduced on all barley cultivars grown next to a flower with stronger pest suppression when all flowers were present. Each flower species recruited a different community of non‐barley aphids that, in turn, varied in their ability to establish the natural enemy populations and subsequently the ability to reduce barley aphid populations. Overall, increased pest suppression in the mixed treatments was a result of numerous weaker interactions between different flower, aphid, and natural enemy species, rather than a few dominant interactions. Natural enemy communities could be enhanced by incorporating flower species that vary in their ability to attract and host alternative prey (i.e., non‐pest aphids) as well as suitable nectar provisioning. We can use our knowledge of ecological interactions to tailor floral plantings to increase the effectiveness of pest control services.     

Entomopathogenic potential of fungi isolated from intertidal environments against the cabbage aphid Brevicoryne brassicae (Hemiptera: aphididae)

The use of biopesticides formulated from entomopathogenic fungi is a strategy utilised in integrated pest management programmes. The microorganisms used in these biopesticides are isolated from terrestrial organisms and ecosystems. However, bioprospecting in marine environments may lead to the discovery of promising fungi for pest control. In this study, marine fungi were identified and evaluated for the control of Brevicoryne brassicae. The effects of the most virulent isolate so identified on the mortality of aphids were compared to the effects of bioinsecticides that were formulated from fungal strains of Beauveria bassiana (Bovemax®) and Metarhizium anisopliae (Methamax®). Moreover, lethal and sublethal effects of this isolate on B. brassicae biological parameters were also examined. The isolates were identified as Aspergillus versicolor, Aspergillus sydowii (isolates 1 and 2), Penicillium dipodomyicola, and Trichoderma harzianum. The fungal strain A. versicolor was the most virulent fungal species, causing 85.9% mortality in B. brassicae at 24 h. The mortality rate caused by A. versicolor was similar to that caused by Bovemax® and Methamax® at concentrations of 10⁵ conidia mL^?1, and superior to that caused by Methamax® at a concentration of 10⁹ conidia mL^?1. The exposure of B. brassicae to CL₂₅ (0.32 × 10³) of A. versicolor did not affect the net reproductive rate (R_o), average generation time (T), intrinsic rate of population growth (r_m), and finite rate of population increase (λ). This is the first study to demonstrate that A. versicolor isolated from a marine environment is a promising candidate for the biological control of agricultural pests.     

Silencing of a lipase maturation factor 2‐like gene by wheat‐mediated RNAi reduces the survivability and reproductive capacity of the grain aphid,Sitobion avenae

Lipase maturation factor (LMF) family proteins are required for the maturation and transport of active lipoprotein lipases. However, the specific roles of LMF2 remain unknown. In this study, a grain aphid lmf2‐like gene fragment was cloned and was highly similar in sequence to a homologous gene in the pea aphid, Acyrthosiphon pisum. An RNAi vector was constructed with this fragment and used for wheat transformation. The expression of the lmf2‐like gene in aphid, as well as the growth and reproduction of the aphids, was analyzed after feeding on the transgenic wheat. There were no significant differences in the expression of the lmf2‐like gene over development. The expression of the lmf2‐like gene was significantly reduced by 27.6% on the fifth day, and 57.6% on the 10th day after feeding. The total number of aphids produced on the transgenic plants was less than the number produced on control plants, and the difference became significant or after 2 weeks. The molting numbers were also reduced in the aphids reared on the transgenic plants. Our findings indicate that lmf2‐like genes may have potential as a target gene for the control of grain aphids and show that feeding aphids with wheat expressing lmf2‐like RNAi resulted in significant reductions in survival and reproduction.     

Manipulating field margins to increase predation intensity in fields of winter wheat (Triticum aestivum)

The effectiveness of natural enemies to control pests can be enhanced through habitat manipulation. However, due to the differences in their ecology, generalist and specialist species may respond differently to the same manipulation. Moreover, interactions among natural enemies (i.e. cannibalism, intraguild predation, hyperparasitism) may complicate the assumption that a higher density of natural enemies would increase the level of biological control. We investigated the natural enemy guild composition and the predation rate along flower vs. grass margins at the edge of winter wheat (Triticum aestivum) fields in Denmark. Natural enemies were sampled by pitfall trapping and by suction sampling; predation intensity was measured using two different sentinel prey methods: artificial caterpillars made of plasticine, and sentinel aphid colonies. Specialist and generalist species responded differently to the two margin types: specialists (mostly parasitic wasps) were attracted by the flower margins, while generalists (ground beetles, rove beetles and spiders) were more active in grass margins. The number of artificial caterpillars attacked was significantly greater in grass margins (mean = 48.9%, SD = 24.3) than in flower margins (mean = 30.7%, SD = 17.4). We found a significant positive relationship between the number of artificial caterpillars attacked by chewing insects, and activity density for large (≥15 mm) ground beetles. Predation of sentinel aphids in wheat fields did not vary significantly in relation to margin type. Our results suggest that flowering margins may be beneficial for canopy‐active specialist natural enemies, but grassy margins are more useful for ground‐active generalist predators.     

Large‐scale gene expression reveals different adaptations of Hyalopterus persikonus to winter and summer host plants

Host alternation, an obligatory seasonal shifting between host plants of distant genetic relationship, has had significant consequences for the diversification and success of the superfamily of aphids. However, the underlying molecular mechanism remains unclear. In this study, the molecular mechanism of host alternation was explored through a large‐scale gene expression analysis of the mealy aphid Hyalopterus persikonus on winter and summer host plants. More than four times as many unigenes of the mealy aphid were significantly upregulated on summer host Phragmites australis than on winter host Rosaceae plants. In order to identify gene candidates related to host alternation, the differentially expressed unigenes of H. persikonus were compared to salivary gland expressed genes and secretome of Acyrthosiphon pisum. Genes involved in ribosome and oxidative phosphorylation and with molecular functions of heme–copper terminal oxidase activity, hydrolase activity and ribosome binding were potentially upregulated in salivary glands of H. persikonus on the summer host. Putative secretory proteins, such as detoxification enzymes (carboxylesterases and cytochrome P450s), antioxidant enzymes (peroxidase and superoxide dismutase), glutathione peroxidase, glucose dehydrogenase, angiotensin‐converting enzyme, cadherin, and calreticulin, were highly expressed in H. persikonus on the summer host, while a SCP GAPR‐1‐like family protein and a salivary sheath protein were highly expressed in the aphids on winter hosts. These results shed light on phenotypic plasticity in host utilization and seasonal adaptation of aphids.     

Bacteria may contribute to distant species recognition in ant–aphid mutualistic relationships

Mutualistic interactions between ant and aphid species have been the subject of considerable historical and contemporary investigations, the primary benefits being cleaning and protection for the aphids and carbohydrate‐rich honeydew for the ants. Questions remained, however, as to the volatile semiochemical factor influencing this relationship. A recent study highlighted the role of bacterial honeydew volatile compounds in ant attraction. Here, ant's ability to distantly discriminate 2 aphid species was investigated based on bacterial honeydew semiochemicals emissions using a two‐way olfactometer. Both the mutualistic aphid Aphis fabae L. and the nonmyrmecophilous aphid Acyrthosiphon pisum Harris were found to be attractive for the ant Lasius niger L. The level of attraction was similar in both assays (control vs. one of the aphid species). However, when given a choice between these 2 aphid species, ants showed a significant preference for Aphis fabae. Honeydew volatiles, mostly from bacterial origins, are known to be a key element in ant attraction. Using the same olfactometry protocol, the relative attractiveness of volatiles emitted by honeydews collected from each aphid species and by bacteria isolated from each honeydew was investigated. Again, ants significantly preferred volatiles released by Aphis fabae honeydew and bacteria. This information suggests that microbial honeydew volatiles enable ants to distantly discriminate aphid species. These results strengthen the interest of studying the occurrence and potential impact of microorganisms in insect symbioses.     

Characterization of polymorphic microsatellite loci in the aphid species Macrosiphum euphorbiae (Hemiptera: Aphididae)

Fourteen microsatellite loci were isolated and characterized in the potato aphid, Macrosiphum euphorbiae Thomas, by screening a genomic library with the oligonucleotide probes (GA)₁₀ (GT)₁₀ and (GATA)₄. Allelic diversity was estimated in samples collected from potato fields in Tunisia. Ten loci displayed polymorphism that ranged from two to four alleles per locus and the observed heterozygosity ranged from zero to one. These markers could be used to study the population genetic structure of this polyphagous aphid species.     

Potential for biotic interference of a classical biological control agent of the soybean aphid

The degree to which resident biota can inhibit the ability of an introduced biological control agent to establish and be effective is termed biotic interference. Studying biotic interference prior to a release using the actual agent is logistically difficult, however, due to quarantine restrictions. An alternative solution is to study biotic interference against a surrogate species in the intended range of introduction, with the expectation that biotic interference against the actual agent will be similar. This study assessed how biotic interference, mostly by generalist predators, may affect establishment of classical biological control agents of the soybean aphid, Aphis glycines Matsumura, in North America. The parasitoid Aphidius colemani Viereck was used as a surrogate for Asian aphidiine braconids such as Binodoxys communis (Gahan). We conducted a factorial field experiment that measured the effect of releasing A. colemani and of excluding resident natural enemies using field cages on soybean aphid populations. We also conducted molecular gut-contents analyses on predators collected in release plots to determine which species fed upon A. colemani. Releasing A. colemani in open field plots increased soybean aphid control beyond that observed in open field plots alone, despite indications that intraguild predation of A. colemani occurred. Thus, biotic interference was not sufficient to eliminate the contribution of A. colemani on soybean aphid suppression during the course of our experiment. Molecular gut-contents analysis revealed that at least two predators, Harmonia axyridis (Pallas) and Chrysoperla carnea Stephens, engaged in intraguild predation against A. colemani. The prolonged effect of intraguild predation on parasitoid establishment remains to be determined.     

Antioxidative enzymes and the Russian wheat aphid (Diuraphis noxia) resistance response in wheat (Triticum aestivum)

A crucial function of antioxidative enzymes is to remove excess reactive oxygen species (ROS), which can be toxic to plant cells. The effect of Russian wheat aphid (RWA), Diuraphis noxia (Mordvilko), infestation on the activities of antioxidative enzymes was investigated in the resistant (cv. Tugela DN) and the near-isogenic susceptible (cv. Tugela) wheat (Triticum aestivum L.). RWA infestation significantly induced the activity of superoxide dismutase, glutathione reductase and ascorbate peroxidase to higher levels in the resistant than in susceptible plants. These findings suggest the involvement of antioxidative enzymes in the RWA-wheat resistance response, which was accompanied by an early oxidative burst. The results are consistent with the role of ROS in the resistance response and the control of their levels to minimise toxic effects.     

Grain aphid population structure: no effect of fungal infections in a 2-year field study in Denmark

1 Sitobion avenae (F.) is a serious pest in Danish cereal crops. To understand the population genetic structure, aphids were sampled in seven different winter wheat (Triticum sativum Lamarck) fields throughout Denmark. The aphids were genotyped with seven microsatellite markers. In total, 2075 aphids were collected and 1203 of these were genotyped. 2 The Danish S. avenae populations displayed very high genotypic diversity, high percentages of unique genotypes and low linkage disequilibria; this is likely to be a result of genetic recombination encompassed by their holocyclic lifestyle. The populations showed very limited differentiation and no sign of isolation by distance. Almost all the genetic variation was ascribed within the populations rather than between populations, probably due to a high migration rate at approximate 10% per generation. 3 Seasonal changes in clonal diversity and distribution of asexual summer generations of S. avenae within the infestation period in a single winter wheat field were followed over two consecutive years by weekly sampling from 60 plots each of 20 × 20 m. Clonal diversity was high in all samples with no dominant clonal lineages and no significant difference in the genotypic diversity between weeks or between years. However, a temporal genetic differentiation effect, throughout the infestation, suggests that selective factors or high temporal migration play an important role in shaping the genetic structure S. avenae. 4 Analyses of fungal infected and uninfected aphids were performed to test whether some clonal linage were more often infected by fungi from the Entomophthorales under field conditions. In total, 54 progeny from aphids with Entomophthorales were genotyped and compared with 422 uninfected aphid genotypes. The Entomophthorales‐infected aphid genotypes did not cluster out together, suggesting that these fungal pathogens did not affect the population differentiation or clonal distribution of S. avenae in a Danish agroecosystem. 5 Our findings indicate that S. avenae populations can be controlled using conservation biological control