Yellow mutant of the Neotropical green lacewing Chrysoperla externa: trait inheritance and predator performance

The Neotropical green lacewing Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) is a key predator of various small soft‐bodied pest species. Chrysopidae species are known as ‘green lacewings’ due to their overall green body coloration. However, yellow mutant individuals were observed emerging from our lacewing rearing colony. Thus, the mode of inheritance of the yellow trait was studied and the hypothesis of an autosomal recessive allele for yellow color was tested using hybridization and backcrossing techniques. Furthermore, the possible implications of this color variation on specific life‐history characteristics of C. externa and the predation rates of each morph were evaluated. In both yellow and green morphs, basic life‐history characteristics were monitored, including time to hatching and viability of eggs, duration, and viability of larval and pupal stages, emergence rate and survivorship of adults, and fecundity and longevity of females. The yellow and green morphs were indistinguishable with respect to all life‐history traits evaluated and the predation rate of their larvae. Crossing experiments revealed the yellow color to be caused by a homozygous recessive allele, without sex‐linked expression. We conclude that the allele for yellow color is occurring at high frequency in the laboratory colony, supporting the existence of a genetic polymorphism for body ground color.     

Manipulation of oviposition and overwintering site choice of common green lacewings with synthetic lure (Neuroptera: Chrysopidae)

Common green lacewings (Chrysoperla carnea species complex) are important predators of several insect pests, particularly aphids. Due to their potential in biological control, several efforts have been made to find means to retain common green lacewing adults or even to increase their numbers at a given site. In the course of field experiments conducted in Hungary and Norway, we tested the effect of a known ternary bait (phenylacetaldehyde, methyl salicylate, acetic acid) on oviposition and overwintering site choice of common green lacewings. In an orchard in Hungary, overwintering chambers were set up with and without baits. For the experiment on oviposition in Norway, a number of lacewing eggs were compared on trees with and without baits in selected sectors of the canopy. With the ternary bait, more common green lacewings could be attracted to overwintering chambers, and also significantly more eggs were found in the vicinity of baits than in other selected parts of the canopy, suggesting that this bait has the potential to manipulate both overwintering site choice and oviposition site choice of these important beneficial insects.     

Semiochemicals and habitat manipulation to support green lacewing activity to reduce aphid infestations in agroecosystems

Conservation biological control (CBC) is a promising tool for ecological intensification that aims to establish resilient natural enemy populations that contribute to pest management with reduced use of pesticides and at the same time support native biodiversity in agroecosystems. Yet the impact of natural enemies in CBC is often limited due to missing resources such as food, habitat, and hibernation shelters. Here, we studied a CBC strategy that incorporates these essential resources combined with semiochemicals, focusing on how the common green lacewing can enhance biological control of aphids.In a 4-year field study conducted at three locations in the region of East Norway, we developed a CBC strategy combining the three measures ATTRACT (a ternary attractant that increase lacewing egg laying), FOOD (floral buffer strips), and SHELTER (insect hotels for overwintering survival) to increase aphid biological control in spring barley. We recorded the number of lacewings, ladybirds, hoverflies, parasitized aphid mummies, and the two cereal aphid species Sitobion avenae and Rhopalosiphum padi. Our CBC strategy resulted in a significant increase in lacewing activity and significant aphid suppression. At all three locations and over the 4-year period, aphid infestation was below the economic damage threshold in the field plots using CBC measures. In contrast, during two of the years, the density of the aphid infestation in the control plots was significantly above the damage threshold. We found evidence that use of the ternary attractant supported green lacewings but led to loss of ladybirds, hoverflies, and parasitoids, even though flower strips were used as alternative resources.Our study shows a promising increase in lacewing activity in the agricultural landscape and high biological control of aphids in barley. Long-term field studies are needed to evaluate the impact on non-target species and the agroecosystem before practical application of this approach can be considered.     

Prey consumption and development of the indigenous lacewing Chrysoperla externa feeding on two exotic Eucalyptus pests

ABSTRACT

The green lacewing Chrysoperla externa is a widespread species in the Neotropical region that occurs in different habitats. Its presence in Eucalyptus plantations infested with Glycaspis brimblecombei (Hemiptera: Aphalaridae) and Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) suggests that this lacewing might feed on one or both exotic pest species. In order to evaluate C. externa as a potential biocontrol agent of the eucalyptus pests, the prey consumption, development, survival and reproduction of the predator were evaluated under laboratory conditions. C. externa larvae consumed nymphs of both pest species. Developmental time and reproduction parameters of C. externa fed G. brimblecombei were similar to those obtained with the factitious prey Sitotroga cerealella. When fed on T. peregrinus, C. externa showed a delay in its developmental time and the emerged adults were malformed. The results of this study suggest that the green lacewing is a good candidate to be used in augmentative or conservative biological control programmes against G. brimblecombei. Further research is necessary to analyse the potential of this predator as a biocontrol agent under field conditions.     

Impact of Cheiracanthium pelasgicum (Araneae: Miturgidae) and Chrysoperla carnea (Neuroptera: Chrysopidae) intraguild predation on the potential control of cotton pest Helicoverpa armigera (Lepidoptera: Noctuidae)

Antagonist interactions such as intraguild predation (IGP) or cannibalism among predatory arthropods can reduce the impact of these invertebrates on pest limitation in agroecosystems. Here, the effects of IGP between two major natural enemies of cotton pests, the cursorial spider Cheiracanthium pelasgicum (C.L. Koch) and the common green lacewing Chrysoperla carnea (Stephens), were studied under laboratory conditions. First, a feeding preference test was carried out to determine the degree of C. pelasgicum preference for lacewing larvae, using second-instar Helicoverpa armigera larvae as alternative prey. In a second bioassay, the effects of predator interactions on potential predation of H. armigera larvae were analysed using three treatment combinations (plus a control with no predator): (1) spider alone, (2) lacewing larvae alone, (3) spider + lacewing larvae. Potential predation by C. pelasgicum on lacewing eggs was also studied. C. pelasgicum showed no significant preference for either of the two species, indicating that this spider may impact negatively on the green lacewing population. Findings revealed no additive effects and an antagonist interaction between C. pelasgicum and green lacewing larvae, which adversely affected H. armigera suppression; both predators displayed lower predation rates when kept together than either predator alone. However, presence of lacewing larvae and subsequent unidirectional IGP did not affect the predation capacity of C. pelasgicum. Finally, predation rates of C. pelasgicum on lacewing eggs were very low (mean 2.35 ± 0.71 eggs, 24 h after offering) indicating that the impact of C. pelasgicum on lacewing populations may be limited.     

Oviposition response of green lacewings (Neuroptera: Chrysopidae) to aphids (Hemiptera: Aphididae) and potential attractants on pecan

Pecan foliage is attacked by three species of aphids [Monellia caryella (Fitch), Melanocallis caryaefoliae (Davis), and Monelliopsis pecanis Bissell], resulting in damage that can reduce tree nut yield. In this study, we assayed the ovipositional response of the green lacewing Chrysoperla rufilabris (Burmeister) to M. caryella and M. caryaefoliae at high and low aphid densities and the development of C. rufilabris larvae when fed solely on each of the three pecan aphid species. During 2004 and 2005, combinations of attractants and food sprays were applied to pecan trees in an orchard to monitor green lacewing ovipositional response. We found that C. rufilabris laid more eggs on seedling trees infested with the M. caryella (at both high and low densities) than on seedlings infested with M. caryaefoliae. Development of C. rufilabris was unaffected by aphid species. At least one attractant/food spray treatment applied to trees in an orchard significantly increased green lacewing oviposition for three of the five treatment dates over both years. These results show that larvae of C. rufilabris will consume all aphid species attacking pecan, even though female ovipositional response can differ for aphid species. It is likely that combinations of attractants and food sprays can be used to enhance green lacewing populations in orchards.     

Pollen Ingestion by <Emphasis Type="Italic">Chrysoperla externa</Emphasis> (Hagen) Adults in a Diversified Organic Agroecosystem

Chrysoperla externa (Hagen) larvae prey on pest insects and mites in agroecosystems, and adults mainly feed on pollen, nectar, and honeydew. Therefore, preserving this lacewing in crop systems depends on having plants that provide these resources. The objectives of this research were to identify pollen grains ingested by Ch. externa adults collected in a diversified organic agroecosystem and to evaluate whether there is a difference in the amount of ingested pollen grains between males and females. The adults of Ch. externa were collected in four different crops during 13 months in Seropédica, state of Rio de Janeiro, Brazil, using a collecting net. The adults were killed and underwent acetolysis, in order to recover the pollen in the gut. A total of 37,441 pollen grains from 19 Angiospermae families were found, besides 16 Pteridophyte spores. Among the recognized pollen grains, those of Poaceae were the majority, both in frequency of occurrence (87.5%) and in quantity (33496), and were found and recovered in every month of collection. Females and males ingested, respectively, 71.9 and 28.1% of the total number of Angiospermae pollen grains consumed by both sexes. The highest number of Poaceae pollens was obtained from the females (72.1% of the total number of Poaceae pollen, recovered from females + males). Taken as a whole, this study showed that adults of Ch. externa find possibilities to maintain throughout the year, in different crops, but the main source of pollen to males and females was Poaceae plants.     

THE ROLE OF COURTSHIP SONGS IN REPRODUCTIVE ISOLATION AMONG POPULATIONS OF GREEN LACEWINGS OF THE GENUS CHRYSOPERLA (NEUROPTERA: CHRYSOPIDAE)

Male and female lacewings tremulate during courtship, establishing duets that always precede copulation. Three distinct courtship songs are found in populations of the green lacewing Chrysoperla plorabunda (P1, P2 and P3 song morphs). Analysis of five features of the songs for individuals collected from Connecticut, Idaho, Oregon and California showed few differences within song morphs, but sympatric song morphs differed significantly in temporal features of the songs and their mode of presentation. Playback experiments using recorded songs were performed on females with all possible sympatric and allopatric combinations of females and recorded songs. The results showed that females strongly prefer to duet with recordings of males of their own song type and usually showed no responses to songs of other types. Thus, song differences are effective barriers to reproduction between the sympatric morphs. Our results support the hypothesis that the three song morphs are true biological species.     

Diversity of lacewing assemblages (Neuropterida:Neuroptera) in different forest habitats and agricultural areas in the East Mediterranean area of Turkey

The objectives of this study were to understand lacewing diversity patterns and the role of environmental factors in determining lacewing diversity in four habitat types: agricultural area (crops and orchards), pine forest (Pinus nigra Arnold and, Pinus brutia Ten), natural forest (cedar and willow‐oak), and mixed forest (beech and oak). Several diversity patterns were evaluated, including evenness and dominance, in the East Mediterranean area of Turkey by analyzing the abundance and species composition of lacewing assemblages using the Simpson and Shannon Diversity Indices. It was questioned whether these communities are structured according to environmental conditions such as altitude, temperature, rainfall, wind and humidity. This question was explored using generalized linear models (GLMs) and principal component analysis (PCA) to detect the effect of ecological parameters on the species composition of the lacewing assemblages. The data suggest that the species abundance, composition, and diversity of lacewings are affected by different forest and agricultural habitat types. Based on the results of the present study, it is recommended that the area of farmland under cultivation is decreased and the area of sustainably managed forest and agricultural land is increased in order to better protect lacewing diversity in the East Mediterranean area of Turkey.     

Spatio-temporal dynamic of green lacewings (Neuroptera: Chrysopidae) taxocenosis on natural ecosystems

In order to study the interactions of green lacewings toxocenosis on natural ecossystems, samplings were carried out in the Parque Ecológico Quedas do Rio Bonito, located in Lavras, Alto Rio Grande region, South of Minas Gerais, Brazil. The species inventory was accomplished in two vegetation types: semi-evergreen forest and open field formations, including areas of montane grassland, rocky montane grassland and "cerrado". Insects were captured with a butterfly net during 2h, walking through each vegetation formation. Sampling resulted in 1,948 specimens belonging to 30 species, of which 14 were Chrysopini and 16 Leucochrysini. Representatives of these tribes were observed both in forest and in open field formations. Species of the genera Ceraeochrysa, Chrysoperla, Chrysopodes, Plesiochrysa and Leucochrysa were found in forests and in open field formations, except for Plesiochrysa. The highest richness and diversity of species were observed in the forest. The similarity index among the communities of green lacewings in the studied areas was 27%.     

The inheritance of mating songs in two cryptic,sibling lacewing species (Neuroptera: Chrysopidae: Chrysoperla)

Speciation often involves incremental responses to natural selection and results in large scale genomic changes, but it may also occur abruptly and with little genetic imprint, as seen in some complexes of cryptic species. Recent attention has focused on sexual selection in rapid speciation, because it can disrupt premating signals that mediate reproductive isolation. Some models require that environmental adaptation assist sexual selection during speciation, while others show that populations can diverge through mate choice alone. We propose that speciation involving environmental adaptation in premating signals is likely to have a polygenic basis, while speciation due to arbitrary changes in premating signals could be accompanied by changes at just a few loci. The sibling species Chrysoperla plorabunda and Chrysoperla johnsoni belong to a large complex of cryptic species of green lacewings, and meet all criteria for speciation via sexual selection. We perform a genetic analysis of line crosses between them, focusing on their substrate-borne premating songs. Measurements of seven song features and their principal components are compared among parentals, F₁ and F₂ hybrids, and backcrosses. The distributions of phenotypes are consistent with a model of more than one, but not many, genes. Sex linkage and/or maternal effects are negligible. C. plorabunda is dominant for most traits affecting mate choice. Bayesian analyses of segregation variance show significant additive and epistatic effects on line means. A Bayesian Castle–Wright estimate suggests that relatively few effective factors are responsible for variation in volley period ( ), number of volleys per song ( ), and PC-1 ( ). Our results are consistent with simple genetic architecture of songs, supporting a role for major genes in premating isolation and strengthening the notion that mate choice alone, without significant environmental adaptation, has been responsible for generating new lacewing species.     

Ontogenetic change of prey preference in the generalist predator Zelus renardii and its influence on predator–predator interactions

1. Two field experiments were conducted to test the hypothesis that the intensity of predation by a generalist predator on two species of prey changes with the developmental stage of the predator. The generalist predator studied was Zelus renardii Kolenati (Hemiptera: Reduviidae) and the prey were the lacewing larva, Chrysoperla carnea Stephens, and the cotton aphid, Aphis gossypii Glover.
2. Zelus renardii and lacewings feed on aphids, thereby acting as potential competitors. In addition, Z. renardii feeds on lacewings. Thus, Z. renardii is an intraguild predator of lacewings.
3. Zelus renardii exhibited changes in prey preferences across developmental stages. The older stages of Z. renardii exerted greater mortality on lacewings and fed on larger lacewing larvae than did the younger stages.
4. Lacewings suppressed aphid population growth strongly. In contrast, none of the stages of Z. renardii was an effective control agent of the cotton aphid.
5. The addition of Z. renardii frequently disrupted the effective control of aphids generated by lacewings. In one of the two replicates of the experiment, the disruption increased with the developmental stage of Z. renardii , paralleling the increase in lacewing mortality.
6. Although the developmental stage of Z. renardii can influence the prevalence of intraguild predation and the intensity of the disruption of the aphid biological control, these experiments have demonstrated that even the youngest instars of Z. renardii can cause substantial lacewing mortality and release aphid populations from regulation.     

Phylogeny of the green lacewing Chrysoperla nipponensis species‐complex (Neuroptera: Chrysopidae) in China,based on mitochondrial sequences and AFLP data

Abstract Several studies have indicated that the green lacewing, Chrysoperla nipponensis (Neuroptera: Chrysopidae) may include more than one valid species. We investigated the phylogenetic status of Chrysoperla nipponensis s.l. in China and Japan using mitochondrial sequences and AFLP data. The molecular phylogenetic analyses based on mitochondrial genes showed that the C. nipponensis species‐complex comprises four clades, each having high support values. In addition, the phylogenetic tree based on AFLP data indicates that the species‐complex comprises three groups. These results confirm that C. nipponensis s.l. comprises at least three genetically distinct clades and suggests that two of these clades may be closely related to populations of C. nipponensis in Japan. However, these clades cannot be recognized as species until analysis of their courtship songs has been completed.     

Influence of larval food consumption on the fecundity of the lacewingChrysoperla carnea

The effects of food consumption on larval growth and development and adult fecundity of the common green lacewing,Chrysoperla carnea (Stephens), were studied on two populations of larvae derived from either a laboratory colony or from field-collected adults. The number of eggs of the Mediterranean flour moth,Anagasta kuehniella (Zeller), provided to individual lacewing larvae was varied to produce three food-supply treatments: low, intermediate, and high. Food-supply was found to influence larval growth and development and adult fecundity. Lacewing larvae provided with an overabundance of moth eggs developed faster than larvae provided with fewer moth eggs than they could have consumed. Adult females that developed from the high feeding treatment had a substantially shorter preoviposition period, a later decline in egg deposition, and a significantly higher fecundity than adults arising from the other feeding classes. Unrestricted feeding by adult lacewings on an artificial diet did not compensate for prior low feeding regimes. The overall performance of the lacewings derived from the laboratory colony was substantially poorer than that of the lacewings derived from field-collected adults. This effect was accentuated when the larvae were given a low food-supply. This overall decrease in vigor is attributed to inbreeding of the laboratory culture over a one year period. These finds are relevant to mass rearing programs for this biological control agent.     

Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population

We evaluated the influence of intraguild predation among generalist insect predators on the suppression of an herbivore, the aphid Aphis gossypii, to test the appropriateness of the simple three trophic level model proposed by Hairston, Smith, and Slobodkin (1960). We manipulated components of the predator community, including three hemipteran predators and larvae of the predatory green lacewing Chrysoperla carnea, in field enclosure/exclosure experiments to address four questions: (1) Do generalist hemipteran predators feed on C. carnea? (2) Does intraguild predation (IGP) represent a substantial source of mortality for C. carnea? (3) Do predator species act in an independent, additive manner, or do significant interactions occur? (4) Can the experimental addition of some predators result in increased densities of aphids through a trophic cascade effect? Direct observations of predation in the field demonstrated that several generalist predators consume C. carnea and other carnivorous arthropods. Severely reduced survivorship of lacewing larvae in the presence of other predators showed that IGP was a major source of mortality. Decreased survival of lacewing larvae was primarily a result of predation rather than competition. IGP created significant interactions between the influences of lacewings and either Zelus renardii or Nabis predators on aphid population suppression. Despite the fact that the trophic web was too complex to delineate distinct trophic levels within the predatory arthropod community, some trophic links were sufficiently strong to produce cascades from higher-order carnivores to the level of herbivore population dynamics: experimental addition of either Z. renardii or Nabis predators generated sufficient lacewing larval mortality in one experiment to release aphid populations from regulation by lacewing predators. We conclude that intraguild predation in this system is wide-spread and has potentially important influences on the population dynamics of a key herbivore.     

Target-oriented dissemination of Beauveria bassiana conidia by the predators,Harmonia axyridis (Coleoptera: Coccinellidae) and Chrysoperla carnea (Neuroptera: Chrysopidae) for biocontrol of Myzus persicae

Dissemination of microbial biocontrol agents via predators may have advantages for safe spore dispersal to targeted pests with the added benefit of predation. A laboratory study was conducted to test the target-oriented dissemination of conidia of Beauveria bassiana using larvae of both the multicoloured Asian lady beetle (Harmonia axyridis) and common green lacewing (Chrysoperla carnea) for control of aphids. Maximum dry conidial attachment occurred within approximately 7 min after exposure. After release of the treated predators on leaves of Chinese cabbage, within 12 hours lacewing larvae dispersed 89% of the attached conidia while Asian lady beetles dispersed 93%. Both predators dispersed conidia up to 2.4 m from the release site. Leaf disk bioassays were conducted to compare two application methods; the dissemination of conidia of B. bassiana by predators and the direct application of conidial suspensions. Mortality in sprayed aphids was 91±2.1% compared to 88±2.1 and 84±4.2%, respectively, when conidia were disseminated by lacewings and lady beetles. Predation was not affected in treated lacewing larvae whereas there was a 20% reduction in predation by lady beetle larvae. It appears that B. bassiana can be effectively delivered using certain insect predators.     

Assessment of fennel aphids (Hemiptera: Aphididae) and their predators in fennel intercropped with cotton with colored fibers

The fennel aphid, Hyadaphis foeniculi (Passerini) (Hemiptera: Aphididae) is a major pest of fennel, Foeniculum vulgare Miller in northeast region of Brazil. We hypothesize that intercropping can be used as an alternative pest management strategy to reduce aphid yield loss in fennel. Thus, we investigated the severity of fennel plant damage in relation to infestation by the fennel aphid and predation by Cycloneda sanguinea (L.) (Coleoptera: Coccinellidae) (spotless lady beetle), green lacewing, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and Scymnus spp. (Coleoptera: Coccinellidae) in sole fennel plots and plots of fennel intercropped with cotton with colored fibers. The fennel aphid populations in nontreated plots were significantly larger in sole fennel plots than in intercropped plots. The highest densities of C. sanguinea, green lacewings and Scymnus spp., associated with the suppression of fennel aphid populations was found in fennel in the intercropping systems. Fennel aphids reduced the fennel seed yield by 80% in the sole fennel plots compared with approximately 30% for all intercropping systems. The results obtained in this research are of practical significance for designing appropriate strategies for fennel aphid control in fennel-cotton intercropping systems. In summary, intercropping fennel with cotton with colored fibers apparently promoted biocontrol of fennel aphid in fennel.     

Ecological character displacement in competing common green lacewings in Europe: a route to speciation?

Competitive interactions among the three common green lacewing species of the Chrysoperla complex in Europe are presented. Four morphological characters were registered as semi‐quantitative traits to assess variation between populations. Data were obtained from 325 adults originating from 14 locations. A statistical approach was performed in conjunction with observations of ecological traits and a survey of genetic relationships assessed by mitochondrial DNA cytochrome b analysis. The results indicate character displacement in Chrysoperla affinis when living in sympatry with Chrysoperla carnea. The morphological traits of Ch. affinis sympatric with Ch. carnea differ from those of allopatric Ch. affinis, although the genetic distance between those strains was weak. This was associated with a large difference in microhabitats and premating behaviour. Variation in courtship songs manifests a process of speciation within related populations. Thus, that ecological switching can also promote character displacement is supported. This suggests that character displacement acts through phenotypic variability and mediates negative interactions among species. These findings suggest that the highest rate of speciation occurs in groups of species in which competition is the strongest. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 292–300.     

The importance of phenotypic differentiation and plasticity in the range expansion of the annual Atriplex tatarica (Amaranthaceae)

The ability of a species to adapt to sub-optimal conditions at the margin of its distribution range and to cope with environmental stress is considered to be important for its successful geographic expansion. To ascertain the roles of phenotypic differentiation and plasticity in the expansion of the annual Atriplex tatarica, we compared plants from populations found in Marginal and Central areas of the species’ range. We grew these plants under marginal climatic conditions in pots with different types of substrate. We assessed the population genetic structure at five putatively neutral allozyme loci to evaluate whether there was any evidence of reduced genetic diversity in Marginal populations compared to Central ones. We used the Q_ST vs. F_ST approach (while F_ST gives a standardised measure of the genetic differentiation among populations for a genetic locus, Q_ST measures the amount of genetic variance among populations relative to the total genetic variance) to ascertain the roles of adaptive vs. non-adaptive processes on phenotypic differentiation. Plants native to the Marginal area of the species’ range flowered earlier and had a lower shoot mass and a higher reproductive allocation than plants native to the Central part of the species’ range. The Marginal populations of Atriplex tatarica showed lower genetic diversity at allozyme loci and higher phenotypic differentiation than the Central populations. We recorded similar plastic responses to substrates in plants native to both regions. Our results indicate that Marginal populations of expanding A. tatarica maintain the ability to adapt locally and to elicit a plastic response to environmental stress, despite loss of genetic diversity.