Aphidophagous guilds on nettle （Urtica dioica） strips close to fields of green pea, rape and wheat

The common nettle （Urtica dioica L.） is a perennial and cosmopolitan plant species and is known to be the source of food for a great diversity of insects. To understand the importance of the nettle in agro-ecosystems, a field experiment was carried out in an experimental farm at Gembloux （Belgium） to study the effect of nettle margin strips on aphid and aphidophagous populations in close field crops, namely wheat （Triticum aestivum L.）, green pea （Pisum sativum L.） and rape （Brassicae napus L.）. The aphids and related beneficial populations were weekly assessed, from March to August 2005, by visual observations in two plots per field crop. A higher abundance of aphidophagous beneficials was collected in nettle strips when compared to the field crops. Particularly, the presence of predatory anthocorids, mirids and green lacewings was observed on nettle only. Nevertheless, the most abundant aphid predatory family, the Coccinellidae, was distributed in both environments, in nettle strips and in crop fields. The field margin supported a significantly higher density ofHarmonia axyridis than the field crops. In contrast, the field crops, green pea particularly, supported a higher density of Coccinella septempunctata. The distribution of the aphidophagous species, mainly the ladybirds, was discussed in relation to the host plant and related aphid species and their potential effect on integrated pest management.     

Potential value of the fibre nettle <Emphasis Type="Italic">Urtica dioica</Emphasis> as a resource for the nettle aphid <Emphasis Type="Italic">Microlophium carnosum</Emphasis> and its insect and fungal natural enemies

The perennial stinging nettle (Urtica dioica L.) is a wild plant that provides resources for aphid natural enemies and can therefore benefit crop protection. Stinging nettles producing approximately three times more fibre than Standard nettles are under commercial development for fibre production. Here we assess the relative value of Austrian Clone 2, a high fibre nettle variety, as a resource for the nettle aphid Microlophium carnosum (Buckton) and its associated natural enemies. The intrinsic rate of increase of M. carnosum cultured on Clone 2 was not different to that on a Standard nettle nor was there an effect of nettle variety on the susceptibility of this aphid to the entomopathogenic fungus Pandora neoaphidis (Remaudière and Hennebert) Humber. The development time of the aphidophagous predator Chrysoperla carnea (Stephens) was not affected by the nettle variety on which M. carnosum was cultured whilst the parasitoid Aphidius ervi (Haliday) fed on honeydew produced by M. carnosum infesting both varieties of nettle. Fibre nettle Clone 2 is therefore able to support non-pest aphids and their natural enemies and, if grown widely in the future, may be useful within conservation biological control and a tool within integrated pest management.     

The role of the perennial stinging nettle, Urtica dioica, as a reservoir of beneficial natural enemies

A wide range of natural enemies, including predators, parasites and entomophagous fungi were observed to feed on the stinging nettle aphid, Microlophium carnosum, populations of which increased rapidly in late April and early May. Patches of stinging nettles thus served as an important alternate feeding site for some beneficial natural enemies before pest aphids appeared on cultivated plants. Anthocoridae, Miridae and Coccinellidae were the most abundant specific predators sampled on nettles; only the Coccinellidae appeared to disperse over a defined period to other habitats. The hymenopterous parasites Aphidius ervi and Ephedrus lacertosus parasitized up to 10% of M. carnosum populations in June: two species of the fungus Entomophthora occurred spasmodically. Cutting patches of nettles in May or June had the most striking effect on the species and numbers of Coccinellidae. Cutting in mid-June might increase the numbers and impact of natural enemies on nearby pest infestations.     

Landscape complexity differentially benefits generalized fourth,over specialized third,trophic level natural enemies

The differential loss of higher trophic levels in the face of natural habitat loss can result in the disruption of important trophic interactions, such as biological control. Natural enemies of herbivorous pests in cropping systems often benefit from the presence of natural habitats in surrounding landscapes, as they provide key resources such as alternative hosts. However, any benefits from a biological control perspective may be dampened if this also enhances enemies at the fourth trophic level. Remarkably, studies of the influence of landscape structure on diversity and interactions of fourth trophic‐level natural enemies are largely lacking. We carried out a large‐scale sampling study to investigate the effects of landscape complexity (i.e. the proportion of non‐crop habitat in the landscapes surrounding focal study areas) on the parasitoid communities of aphids in wheat and on an abundant extra‐field plant, stinging nettle. Primary parasitoid communities (3rd trophic level) attacking the cereal aphid, Sitobion avenae, had little overlap with the communities attacking the nettle aphid, Microlophium carnosum, while secondary parasitoids (4th trophic level) showed high levels of species overlap across these two aphids (25 vs 73% shared species respectively), resulting in significantly higher linkage density and lower specialization for secondary than primary parasitoid webs. In wheat, parasitoid diversity was not related to landscape complexity for either primary or secondary parasitoids. Rates of primary parasitism were generally low, while secondary parasitism rates were high (37–94%) and increased significantly with increasing landscape complexity, although this pattern was driven by a single secondary parasitoid species. Overall, our results demonstrate that extra‐field habitats and landscape complexity can differentially benefit fourth, over third, trophic level natural enemies, and thereby, could dampen biological control. Our results further suggest that fourth trophic‐level enemies may play an important, yet understudied, role in linking insect population dynamics across habitat types.     

Intraguild interactions of aphidophagous predators in fields: effect of Coccinella septempunctata and Episyrphus balteatus occurrence on aphid infested plants

Intraguild relations between beneficial insects have become a major research topic in biological pest control. In order to understand the intraguild competitions between aphidophagous populations in natural conditions, a field experiment was carried out in the experimental farm of the Gembloux Agricultural University. As biological control of pests involve a community of diverse natural enemies, this experiment firstly aimed to assess the aphidophagous predator diversity and abundance in green pea (Pisum sativum) field and secondly to investigate the impact of the large natural occurrence of C. septempunctata on the aphidophagous beneficial dispersion and efficiency as aphid biological control agents in pea field. Visual observations were weekly performed throughout the 2006 growing season. The pea aphids were attacked by several predatory groups, mainly ladybird beetles and hoverflies. Higher densities of ladybirds and hoverflies were recorded in the beginning of July, associated with an aphid occurrence peak. Using net cage system in the field, the particular intraguild relations between added C. septempunctata or E. balteatus and the natural beneficial arrivals and dispersion were observed. The E. batteatus (eggs and larvae) presence inhibited other aphidophagous predators presence on the aphid infested plants. Lower abundance of E. balteatus was observed on aphid infested plants already colonised by C. septempunctata. To explore more accurately the oviposition and predation behaviours of ladybirds and hoverflies and to determine the chemical factors that could influence these behaviours, current researches are performed in laboratory and will be discussed to promote efficient biological control of aphids by natural enemies.     

Can competition explain local rarity of a nettle aphid?

Abstract.  1. Previous studies have shown that two aphid species, Microlophium carnosum and Aphis urticata on stinging nettle ( Urtica dioica ) show very different abundance patterns.
2. Theory suggests that the local rarity of A. urticata in Silwood Park, U.K., might be explained by competitive exclusion by the more common species, mediated indirectly through natural enemies. Experimental aphid colonies on potted nettles were used to test for effects of M. carnosum on A. urticata in the field.
3. Though there was some evidence that natural enemies aggregated on the aphid colonies, no population-level effects of competition from M. carnosum on A. urticata could be detected. No evidence was found for competition being a major factor causing the local rarity of A. urticata .     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Increased nitrogen fertilization inhibits the biocontrol activity promoted by the intercropping partner plant

The examination of the compatibility between agricultural practices and biocontrol activities is crucial for establishing an efficient, eco-friendly, and sustainable pest management program. In this study, we examined the population dynamics of two specialist aphids, the English grain aphid (Sitobion avenae) on potted wheat and the pea aphid (Acyrthosiphon pisum) on potted alfalfa, as well as the biocontrol activity of a generalist predator, the harlequin ladybird beetle (Harmonia axyridis). We investigated their responses to the presence of the intercropping partner plant species (alfalfa and wheat, respectively) through plant volatiles or visual cues at three nitrogen fertilizer levels in a greenhouse. In the absence of the predator, the English grain aphid population growth rate increased significantly with increasing nitrogen levels, whereas the pea aphid population increased significantly more slowly in response to high nitrogen levels. The English grain aphid and pea aphid population dynamics were unaffected by the presence of the intercropping partner. However, the presence of the intercropping partner enhanced the control of both aphid populations by the harlequin ladybird beetle. Increasing nitrogen fertilizer levels decreased the predation rates, which were otherwise increased by the intercropping partner. The beneficial effects of the intercropping partner were eventually non-existent at the highest nitrogen level tested. These results imply that the interaction between the presence of intercropping partner and the nitrogen fertilizer application affects the biocontrol activity of the natural enemies of insect pests. Thus, the compatibility between agricultural intensification and biocontrol strategies in integrated pest management programs need to be investigated.     

The population dynamics of the stinging nettle aphid, Microlophium carnosum (Bukt.)

• 1 Populations of Microlophium carnosum on patches of perennial stinging nettle, Urtica dioica increased rapidly during April and May to reach their peaks in June. The decline in numbers was equally rapid and very small populations persisted into autumn; parthenogenetic over-wintering was recorded.
• 2 Suboptimal ambient temperature and mortality due to natural enemies contributed mainly to the post-peak development of aphid populations.
• 3 The combined effects of intraspecific competition and a deterioration in the food quality of the host plant appeared to be the major factors determining the temporal pattern of aphid abundance.
• 4 Variation in the size of populations between the three sampled sites was correlated with differences in the food quality of nettles as indicated by aphid mean relative growth rate.
• 5 Each nettle patch has a particular ‘carrying capacity’ for aphids, within which a biennial fluctuation between relatively large and small aphid populations appeared to be emerging at most of the sites investigated. A natural or aphid-induced cycle in host plant quality, or alternatively, the persistent effects of intraspecific competition over several generations, may explain this fluctuation.

     

Larvae of the exotic predatory ladybird <Emphasis Type="Italic">Platynaspidius maculosus</Emphasis> (Coleoptera: Coccinellidae) on citrus trees: prey aphid species and behavioral interactions with aphid-attending ants in Japan

An aphidophagous ladybird, Platynaspidius maculosus (Weise) (Coleoptera: Coccinellidae), is originally distributed in China, Taiwan, and Vietnam. The ladybird has recently intruded into the southern and central parts of Japan. The present study found that the larvae of this ladybird preyed on three aphid species, Aphis spiraecola, Aphis gossypii, and Toxoptera citricidus (all Hemiptera: Aphididae), feeding on young shoots of various Citrus species in August to early October in Shizuoka Prefecture, central Japan. Laboratory rearing of the sampled larvae confirmed that the larvae completed their development (adult emergence) by consuming each of the three aphid species. The ladybird larvae were observed foraging in aphid colonies attended by one of the four ants, Lasius japonicus, Pristomyrmex punctatus, Formica japonica, and Camponotus japonicus (all Hymenoptera: Formicidae). Field observations revealed that the foraging/feeding larvae were almost completely ignored by honeydew-collecting ants even when they physically contacted each other. Thus, in Japan, the larvae of the exotic ladybird exploit colonies of the three aphid species attended by one of the four ant species on many Citrus species. On the basis of the results, I discuss the possibility of the ladybird’s reproduction on citrus trees in Japan, probable adaptations of the ladybird larvae to aphid-attending ants, and potential impacts of the ladybird on native insect enemies attacking ant-attended aphids on citrus.     

Tri-trophic interactions involving pest aphids,predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance

Transgenic crops genetically engineered for enhanced insect resistance should be compatible with other components of IPM for the pest resistance to be durable and effective. An experimental potato line was genetically engineered to express an anti-aphid plant protein (snowdrop lectin, GNA), and assessed for possible interactions of the insect resistance gene with a beneficial pest predator. These extended laboratory studies are the first to demonstrate adverse tri-trophic interactions involving a lectin- expressing transgenic crop, a target pest aphid and a beneficial aphidophagous predator. When adult 2-spot ladybirds (Adalia bipunctata[L.]) were fed for 12 days on peach-potato aphids (Myzus persicae Sulzer) colonising transgenic potatoes expressing GNA in leaves, ladybird fecundity, egg viability and longevity significantly decreased over the following 2–3 weeks. No acute toxicity due to the transgenic plants was observed, although female ladybird longevity was reduced by up to 51%. Adverse effects on ladybird reproduction, caused by eating peach-potato aphids from transgenic potatoes, were reversed after switching ladybirds to feeding on pea aphids from non-transgenic bean plants. These results demonstrate that expression of a lectin gene for insect resistance in a transgenic potato line can cause adverse effects to a predatory ladybird via aphids in its food chain. The significance of these potential ecological risks under field conditions need to be further evaluated.     

<Emphasis Type="Italic">Aphidius ervi</Emphasis> Preferentially Attacks the Green Morph of the Pea Aphid, <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis>

The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae) is found in red and green color morphs. Previous work has suggested that the aphidiine parasitoid Aphidius ervi Haliday preferentially attacks green pea aphids in the field. It is not clear whether these results reflect a real preference, or some unknown clonal difference, such as in immunity, between the aphids used in the previous studies. We used three susceptibility-matched pairs of red and green morph pea aphid clones to test for preferences. In a no-choice situation, the parasitoids attacked equal proportions of each color morph. When provided with a choice, A. ervi was significantly more likely to oviposit into colonies formed from green morphs when the neighboring colony was formed from red morph aphids. In contrast, red morphs were less likely to be attacked when their neighboring colony was of the green morph. By preferentially attacking green colonies, A. ervi may reduce the likelihood of intraguild predation, as it is suggested that visually foraging predators preferentially attack red aphid colonies. Furthermore, if this host choice behavior is replicated in the field, we speculate that color morphs of the pea aphid may interact indirectly through their shared natural enemies, leading to intraspecific apparent competition.     

The evolution of nettle resistance to heavy deer browsing

We examined whether heavy browsing by sika deer, Cervus nippon Temminck, changed morphological characteristics of a Japanese nettle, Urtica thunbergiana Sieb. et Zucc., in Nara Park, where a large population of sika deer has been maintained for more than 1,200 years. Wild nettles of Nara Park exhibited smaller leaf area, 11–223 times more stinging hairs per leaf, and 58–630-times higher stinging hair densities than those of other areas where there was no evidence of sika deer browsing. There were no significant differences in stinging hair length between the areas. Nettles from Nara Park that were cultivated from seeds in a greenhouse retained a larger number and higher density of stinging hairs. In the field, nettles of Nara Park were less frequently browsed by sika deer and showed higher survivorship than nettles that were transplanted from an unbrowsed area into Nara Park. These results indicate that: (1) the U. thunbergiana population of Nara Park has an extremely high stinging hair density compared with those of unbrowsed areas; (2) this characteristic has a genetic basis, and (3) stinging hairs serve as a defensive structure against sika deer, contributing to an increase in survivorship. Thus, we conclude that a U. thunbergiana population in Nara Park, with extremely high stinging hair densities, has evolved through natural selection due to heavy browsing by sika deer.     

Toxicity of plant essential oil vapours to aphid pests and their coccinellid predators

The comparative toxicity of five essential oil vapours was tested against four aphid species, the black bean aphid Aphis fabae, the pea aphid Acyrthosiphon pisum, the chrysanthemum aphid Macrosiphoniella sanborni, the green peach aphid Myzus persicae and on two of the most common coccinellid predators, the seven-spotted ladybird Coccinella septempunctata and the two-spotted ladybird Adalia bipunctata. All essential oils were highly toxic to the aphid species tested with LC₅₀ and LC₉₉ values ranging between 0.17 and 1.92 and 0.44 and 4.83 µL/L air, respectively, depending on the aphid species and on the essential oil. Coccinellid predators were also highly susceptible to the essential oil vapours and the selective toxicity ratio varied depending on aphid species, coccinellid predator and essential oil. The possibilities for the utililization of essential oils as aphicides, especially in IPM programmes in glasshouses are discussed with regard to the present findings.     

Intra‐specific variation affects the structure of the natural enemy assemblage attacking pea aphid colonies

Abstract 1. Intra‐specific variation in plant defence traits has been shown to profoundly affect herbivore community structure. Here we describe two experiments designed to test whether similar effects occur at higher trophic levels, by studying pea aphid–natural enemy interactions in a disused pasture in southern England. 2. In the first experiment, the numbers and identity of natural enemies attacking different monoclonal pea aphid colonies were recorded in a series of assays throughout the period of pea aphid activity. 3. In the summer assay, there was a significant effect of clone on the numbers of aphidophagous hoverfly larvae and the total number of non‐hoverfly natural enemies recruited. Clone also appeared to influence the attack rate suffered by the primary predator in the system, the hoverfly Episyrphus balteatus, by Diplazon laetatorius, an ichneumonid parasitoid. Colonies were generally driven to extinction by hoverfly attack, resulting in the recording of low numbers of parasitoids and entomopathogens, suggesting intense intra‐guild predation. 4. To further examine the influence of clonal variation on the recruitment of natural enemies, a second experiment was performed to monitor the temporal dynamics of community development. Colonies were destructively sampled every other day and the numbers of natural enemies attacking aphid colonies were recorded. These data demonstrated that clonal variation influenced the timing, abundance, and identity of natural enemies attacking aphid colonies. 5. Taken together, these data suggest that clonal variation may have a significant influence on the patterns of interactions between aphids and their natural enemies, and that such effects are likely to affect our understanding of the ecology and biological control of these insect herbivores.     

Aphid population dynamics: does resistance to parasitism influence population size?

1. Insect population size is regulated by both intrinsic traits of organisms and extrinsic factors. The impacts of natural enemies are typically considered to be extrinsic factors, however insects have traits that affect their vulnerability to attack by natural enemies, and thus intrinsic and extrinsic factors can interact in their effects on population size. 2. Pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in New York and Maryland that are specialised on alfalfa are approximately two times more physiologically resistant to parasitism by Aphidius ervi Haliday (Hymenoptera: Braconidae) than pea aphids specialised on clover. To assess the potential influence of this genetically based difference in resistance to parasitism on pea aphid population dynamics, pea aphids, A. ervi, and other natural enemies of aphids in clover and alfalfa fields were sampled. 3. Rates of successful parasitism by A. ervi were higher and pea aphid population sizes were lower in clover, where the aphids are less resistant to parasitism. In contrast, mortality due to a fungal pathogen of pea aphids was higher in alfalfa. Generalist aphid predators did not differ significantly in density between the crops. 4. To explore whether intrinsic resistance to parasitism influences field dynamics, the relationship between resistance and successful field parasitism in 12 populations was analysed. The average level of resistance of a population strongly predicts rates of successful parasitism in the field. The ability of the parasitoid to regulate the aphid may vary among pea aphid populations of different levels of resistance.     

Natural enemy composition rather than richness determines pest suppression

Natural enemy (NE) biodiversity is thought to play an important role in agricultural pest suppression. However, the relative importance of the number of NE species (species richness), versus the particular combinations of species (species composition), in determining aphid suppression and ultimately crop yields, remains poorly understood. We tested the effects of NE richness and composition on pea aphids Acyrthosiphon pisum (Harris) and broad bean plants Vicia faba (Linn.). We used the larvae of two predator species, the ladybird Adalia bipunctata (Linn.) and the green lacewing Chrysopa carnea (Stephens), and the parasitic wasp Aphidius ervi (Haliday) as enemies. NEs generally reduced aphid density but did not increase final plant biomass, despite a significant negative correlation between aphid density and plant biomass. Among NE treatments, species richness had an inconsistent effect on aphid density. The composition of NEs within richness levels also affected final aphid density: the ladybird was a key species among the treatments in controlling aphid density and was especially effective in combination with the parasitoid. This ladybird/parasitoid combination also appeared to drive the higher level of suppression observed at the two, relative to three, species richness levels. Although these three species of aphid NEs are commonly used in aphid control, this is the first study, to our knowledge, that simultaneously examined these three species and highlighted the composition effect between the A. bipunctata and A. ervi. In conclusion, increasing NE species richness had an inconsistent effect on aphid density. Meanwhile, the presence of a key species (the ladybird) and its combination with a parasitoid was an important determinant of aphid biological control.     

Performance of an aphid Myzus persicae and its parasitoid Diaeretiella rapae on wild and cultivated Brassicaceae

To determine to what extent wild species related to crops might serve as refuges for insect pests and their natural enemies, we compared the performance of the aphid Myzus persicae and its endoparasitoid Diaeretiella rapae on one cultivar of Brassica napus and Brassica oleracea, two wild species Brassica nigra and Sinapis arvensis, and one cultivar of Solanum lycopersicum. These species differ in traits associated with plant defences that may have an impact on the herbivore and its parasitoid. In contrast to our initial hypothesis, aphid population growth rate was significantly smaller on B. napus than on the other Brassicaceae species. Similarly, the performance of the parasitoid was affected by the host plant on which the aphid was feeding. However, aphid and parasitoid performance was not correlated. Thus, in temporally changing landscapes, pests and natural enemies may utilize crops and wild-related host species with contrasting impacts on their fitness.     

Overlapping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids

Oviposition behavior in two co-occurring species of predatory ladybirds of aphids were investigated. The two species of beetles often shared the same aphid colonies in bean plants in space and time and showed a similar oviposition pattern in response to aphid abundance. Overlapping oviposition presents potential risks of interspecific predation of eggs in unstable aphid colonies. Eggs in clusters by two ladybird species, Menochilus sexmaculatus and Coccinella transversalis, were defended from reciprocal predation and the defense was found to be chemical. Eggs occurring singly were found to be highly vulnerable to predation. Strength of chemical defense significantly increased from single eggs to eggs in mixed clusters and eggs in pure clusters. Results are not only consistent with the hypothesis that eggs in clusters are better protected from natural enemies but also extend the ambit of the hypothesis that coexisting ladybird predators have evolved to avoid the risks of heterospecific predation of eggs in a patch. Received: September 11, 2000 / Accepted: November 13, 2000