Native parasitoids and their potential to control the invasive leafminer, Cameraria ohridella DESCH. & DIM. (Lep.: Gracillariidae)

In spite of the fact that since the end of the eighties, the horse chestnut leafminer, Cameraria ohridella, has established itself throughout Europe, native predators such as ants and birds are not attuned to this neozoic species. In contrast, several parasitic wasp species already started to exploit the invasive horse chestnut leafminer, but until now parasitation rates are quite low, mainly because of asynchrony in the lifecycles of parasitoids and host. Only the removal of leaf litter, in which pupae hibernate, is at the moment a strategy to reduce the infestation level in the next year. Unfortunately, not only hibernating horse chestnut leafminers but also parasitoids are removed, and important resources for biocontrol are unused. In the current study, we investigated the potential efficiency of the horse chestnut leafminer parasitoid complex extracted from leaf litter in defined environments. Parasitoids were released at different densities to investigate density dependence in parasitation rates.Although seven different species were released in our experiments, only Pnigalio agraules turned out to be responsible for biocontrol of C. ohridella. We recorded parasitation rates of up to 35%. Overall, parasitation rates were independent of the leafminer density but increased fourfold if ten times more parasitoid individuals were released. Unfortunately, none of the parasitoid species could be established in the experimental units in the long run. Results are compared to other parasitoid-leafminer systems, and promotion of horse chestnut leafminer parasitoids to support natural selection and biological control of the horse chestnut leafminer is discussed.     

How to safely compost Cameraria ohridella-infested horse chestnut leaf litter on private compost heaps

Abstract:  The horse chestnut leafminer Cameraria ohridella (Lep., Gracillariidae) is a recently introduced invasive pest, which frequently defoliates horse chestnut trees Aesculus hippocastanum already in summer. Currently, the removal of leaf litter, in which pupae of C. ohridella hibernate, is the only effective short-term control measure available. In the past the deposition of pest-infested litter on private compost heaps was dissuaded because of the risk of leafminer emergence in the following spring. Thus, the aim of this study was to test safe ways to compost pest-infested horse chestnut leaf litter on small heaps so that private gardeners can save the costs for leaf disposal. The number of C. ohridella adults emerging from heaps covered with either soil or uninfested foliage was reduced by 96% compared with controls. Only single leafminers emerged from the top covered heaps and there was no difference between the use of soil or uninfested foliage as cover. However, cover did not prevent the emergence of a few leafminers over the sides of the heaps. Overall, we conclude that it is relatively safe to compost C. ohridella -infested A. hippocastanum leaf litter on small compost heaps provided they are properly covered.     

Evaluation of the community of native eulophid parasitoids on Cameraria ohridella Deschka and Dimic in urban areas

The parasitoid complex associated with the exotic leafminer Cameraria ohridella Deschka and Dimic (Lepidoptera: Gracillariidae), which attacks horse chestnut (Aesculus hippocastanum L.), was studied in the urban environment of Turin (northern Italy). The studies were carried out over 5 yr after the first detection of the pest in our region in 1999. To evaluate parasitism, 438,029 leaf mines were examined over the 5-yr period, of which 29,033 were found to be parasitized (6.6%). Also, ornamental broadleaf trees attacked by other native gracillariid leafminers and located in the proximity of the target horse chestnut trees were sampled. A total of 11 parasitoid species (Hymenoptera: Eulophidae) were recorded on C. ohridella, and the most common species were Minotetrastichus frontalis (Nees), Closterocerus trifasciatus Westwood, and Pnigalio agraules (Walker). The first species accounted for >77.5% of all parasitoids collected. Cirrospilus talitzkii Boucek was found for the first time in 2005. The high population level of the pest and the low parasitism rate show that the parasitoid complex is currently inadequate to contain C. ohridella populations effectively. The most frequent parasitoids of the moth were also found on the most common broadleaf trees in the studied area, showing how native leafminer parasitoid species are able to switch to other hosts. These results show that both native and broadleaf plants species may potentially provide an important reservoir of parasitic wasps to help protect a simple biotope, such as the urban environment, from pests.     

Possibilities to control the horse chestnut leaf miner (Cameraria ohridella) in urban environments

The continuous epidemic infestation of horse chestnuts by C. ohridella is a serious aesthetic and economic problem in urban environments. The aim of the presented studies was therefore to develop control measures which meet the special needs of urban plant protection. Removal of infested leaves in autumn and appropriate disposal of the leaflitter is the only practicable measure to reduce infestation levels so far. Another two methods, which are currently in an experimental stage, had an impact on the leafminer populations. A gelformulated combination of the C. ohridella-pheromone with a contact insecticide as attract-and-kill-system proved to be efficient at low population levels. Easily applicable and safe banks of systemic insecticides turned out to be effective in killing preimaginal stages of the leafminer on young trees. The complex of parasitoids attacking C. ohridella is comparable to that of other leafminers. Nevertheless, parasitism rates are very low at present and far away from having any controlling effect on the pest insect.     

Sequential sampling plan for Cameraria ohridella (Lepidoptera: Gracillariidae) on horse chestnut tree

A fixed precision sequential sampling plan for estimating the density of the horse chestnut, Aesculus hippocastanum L., leafminer Cameraria ohridella Deschka & Dimic (Lepidoptera: Gracillariidae) was developed. Data were collected from 2002 to 2004 in Turin, northwestern Italy, with the aim of developing a sampling strategy for estimating populations of C. ohridella mines. Taylor's power law was used as a regression model. Sampling parameters were estimated from 216 data sets, and an additional 110 independent data sets were used to validate the fixed precision sequential sampling plan with resampling software. Covariance analysis indicated that there were not significant differences in the coefficient of Taylor's power law between heights of the foliage, months, and years. Dispersion patterns of C. ohridella were determined to be aggregated. The parameters of the Taylor's power law were used to calculate minimum sample sizes and sampling stop lines for different precision levels. Considering a mean density value of five mines per leaf, an average sample number of only 49 leaves was necessary to achieve a desired precision level of 0.25. As the precision level was increased to 0.10, the average sample size increased to 303 leaves. The sequential sampling plan should provide an effective management of C. ohridella in the urban areas, minimizing sampling time and cost, and at the same should be an effective tool to reduce insecticide applications and prevent the esthetic damage.     

Spatial patterns and infestation processes in the horse chestnut leafminer Cameraria ohridella: a tale of two cities

Spatial patterns of the horse chestnut leafminer Cameraria ohridella Deschka & Dimic (Lepidoptera: Gracillariidae) population density was analysed in the cities of Bern and Brussels in order to explore its spatial population dynamics. The surveys were carried out in Bern in 1998 and 2000 and in Brussels in 2001 to assess population density in relation to local characteristics. In Brussels, population density was also measured using pheromone traps distributed over the city and collected twice per moth generation. A quantitative relationship was found between local population density (measured by pheromone traps and survey observations) and the amount of leaves left on the ground the previous fall. Several other factors were related to observed infestation levels: the occurrence of the pathogen Guignardia aesculi was inversely related to infestation by C. ohridella in Bern in 1998 and 2000, the number of horse chestnut trees within 800 m distance was positively related to infestation level in Bern in 2000, and the proportion of green areas within 100 m and the number of other horse chestnut trees within 2000 m were positively related to infestation levels in the 2001 Brussels survey. The pattern of infestation levels as a function of distance to potential population reservoirs suggested that C. ohridella re‐invades areas where overwintering leaves have been cleaned from refuge areas such as parks or urban forests. Our results indicate that the removal of leaves is a feasible first aid control measure to reduce moth population densities. However, leaf removal may not reduce moth densities when done improperly. In places where proper leaf removal is not feasible, other control measures are needed.     

Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae)

Biological invasions usually start with a small number of founder individuals. These founders are likely to represent a small fraction of the total genetic diversity found in the source population. Our study set out to trace genetically the geographical origin of the horse-chestnut leafminer, Cameraria ohridella , an invasive microlepidopteran whose area of origin is still unkown. Since its discovery in Macedonia 25 years ago, this insect has experienced an explosive westward range expansion, progressively colonizing all of Central and Western Europe. We used cytochrome oxidase I sequences (DNA barcode fragment) and a set of six polymorphic microsatellites to assess the genetic variability of C. ohridella populations, and to test the hypothesis that C. ohridella derives from the southern Balkans (Albania, Macedonia and Greece). Analysis of mtDNA of 486 individuals from 88 localities allowed us to identify 25 geographically structured haplotypes. In addition, 480 individuals from 16 populations from Europe and the southern Balkans were genotyped for 6 polymorphic microsatellite loci. High haplotype diversity and low measures of nucleotide diversities including a significantly negative Tajima's D indicate that C. ohridella has experienced rapid population expansion during its dispersal across Europe. Both mtDNA and microsatellites show a reduction in genetic diversity of C. ohridella populations sampled from artificial habitats (e.g. planted trees in public parks, gardens, along roads in urban or sub-urban areas) across Europe compared with C. ohridella sampled in natural stands of horse-chestnuts in the southern Balkans. These findings suggest that European populations of C. ohridella may indeed derive from the southern Balkans.     

An Experimental Study of Predator Recognition in Great Tit Fledglings

Studies of naturally predator-naïve adult birds (finches on predator-free islands) and birds experimentally hand reared in isolation from predators indicate that birds can recognise predators innately; that is, birds show anti-predator behaviour without former experience of predators. To reduce predation risk efficiently during the vulnerable fledgling period, we would predict an innate response to be fully developed when the chicks leave the nest. However, 30-day-old naïve great tit fledglings ( Parus major ) did not respond differently to a model of a perched predator than to a similarly sized model of a non-predator. Although chicks showed distress responses such as warning calls and freezing behaviour, they did not differentiate between the stimuli. In contrast, wild-caught first-year birds (4 mo old) and adults responded differentially to the two stimuli. Lack of recognition of a perched predator might be one explanation for the high mortality rate found in newly fledged great tits. Our results imply that parental care is not only important for food provisioning, but also to reduce predation risk during the time when fledglings are most vulnerable.     

Pathogenicity of entomopathogenic fungi on hibernating pupae of Cameraria ohridella Deschka & Dimic 1986 (Lepidoptera, Gracillariidae). Part 2: Efficacy of entomopathogenic fungi against pupa in her pupal cell

The naked pupae of chestnut leafminer Cameraria ohridella are susceptible for entomopathogenic fungi Paecilomyces fumosoroseus strain P6; Lecanicillium muscarium strain V24; Metarhizium anisopliae strain M72 and Beauveria bassiana strain B412. Their activity at low temperature is advantageous especially for the use in the winter season. (Richter et al., 2007a). Therefore the possibility of infection should be examined in biotest for pupae in their pupal cells on leaf of chestnut at conditions Like in winter. Efficacy of entomopathogenic fungi is decreased, if pupae are in their pupal cells. But fungi, especially L. muscarium, proved the ability to infect pupae of C. ohridella in their pupal cells. Infected pupae moulded in their pupal cells after application. Infection doesn't come from spores. In semi field trials with L. muscarium 60% of pupae were infected in their pupal cells and died after incubation with mouldiness.     

Biocontrol of <Emphasis Type="Italic">Cameraria ohridella</Emphasis> by insectivorous birds in different landscape contexts

The horse chestnut leaf miner (HCLM) Cameraria ohridella Deschka and Dimic (Lepidoptera, Gracillariidae) is a novel but significant pest in Europe. Current control measures are either inefficient or environmentally harmful. Tits (Parus spp.) open the mines and prey on HCLM, but the biocontrol efficiency of this behaviour has not yet been quantified. We installed bird nesting-boxes in a biennial field study on four sites close to Brunswick (Germany). On the same sites, we counted HCLM pupae, larvae, opened and closed mines, and parasitised larvae and pupae in leaves collected from horse chestnut (Aesculus hippocastanum L., Hippocastanaceae) trees with and without bird exclusion. In both years, the HCLM number and the proportion of closed mines were higher in bird exclusion trees, particularly on sites with high abundance of tits. Hence, we suggest including the facilitation of birds, particularly tits, in future HCLM biocontrol strategies.     

Detection distance influences escape behaviour in two parids, Parus major and P. caeruleus

When birds are attacked by aerial predators they should benefit by adjusting their escape to the prevailing attack situation. One important factor likely to affect escape decisions of prey, to our knowledge not previously studied, is the distance at which the attacking predator is detected. We investigated if great tits Parus major and blue tits P. caeruleus alter their escape behaviour to two different detection distances (2.3 m and 1m) by simulating surprise attacks using a predator model. Both species used the information about detection distance when escaping by increasing the escape angle at the shorter detection distance. In addition, blue tits adjusted to the shorter detection distance by dodging sideways more frequently. Great tits escaped initially steeper and faster than blue tits, whereas blue tits increased escape angle and speed more than great tits along the measured distance after taking wing.     

Impact of avian and arthropod predation on lepidopteran caterpillar densities and plant productivity in an ephemeral agroecosystem

Abstract.  1. Most studies evaluating the combined impact of spiders and other predators on herbivore densities in agroecosystems have focused primarily on their trophic connections with invertebrate predators (e.g. carabids, chrysopids); however linkages among spiders and vertebrate predators may also help structure the population dynamics of insect herbivores. A field experiment was conducted to examine the impact of avian and spider predation on lepidopteran caterpillar densities and plant productivity within a Brassica agroecosystem.
2. Arthropod abundance, leaf-chewing damage, and final plant productivity associated with broccoli, Brassica oleracea L. (var. italica ), were recorded for four treatments: (1) bird present but spiders removed; (2) both birds and spiders present; (3) birds excluded, spiders present; and (4) birds and spiders both excluded.
3. Densities of Artogeia rapae L. (Lepidoptera: Pieridae) and Trichoplusia ni Hübner (Lepidoptera: Noctuidae) large caterpillars and post feeding stages were reduced significantly by bird predation. The abundance of large caterpillars was also reduced on spider-inhabited plants during early plant growth; however the assemblage of birds and spiders did not suppress caterpillar densities more significantly than either predator alone.
4. Plants protected by birds, spiders, and birds plus spiders sustained less folivory attributable to leaf chewing caterpillars than check plants. Plant productivity was also greater for predator-protected plants than check plants.
5. Although spiders and parasitoids were responsible for some of the mortality inflicted upon lepidopteran caterpillars, it was concluded that in this study system, birds are the most important natural enemies of folivores.     

Visual, semi-quantitative assessments allow accurate estimates of leafminer population densities: an example comparing image processing and visual evaluation of damage by the horse chestnut leafminer Cameraria ohridella (Lep., Gracillariidae)

Abstract: Qualitative or semi-quantitative visual assessments are most often used for estimating population size of herbivorous insects. The precision of these estimates, however, is often difficult to establish. A 'simulation game' with the horse chestnut leafminer, Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae) shows that visual, semi-quantitative assessments can provide accurate information. Damaged areas of 411 horse chestnut leaves collected in 100 sites were closely related to mine numbers despite some variability in mine and leaf size ( R ² = 0.915; n  = 411; P < 0.001). On the basis of this relationship, two methods of population assessment are compared: (i) digital image processing of leaf damage and (ii) visual assessment using a damage key reflecting the relative infested area on each leaf (0, 0%; 1, 0–2%; 2, 2–5%; 3, 5–10%; 4, 10–25%; 5, 25–50%; 6, 50–75%; 7, 75–100%). Both methods used to estimate damage presented a similar, close relationship to the 'real' numbers of mines ( R ² = 0.858; n  = 777; P < 0.001 for image processing and R ² = 0.905; n  = 777; P < 0.001 for visual assessment). The potential of using visual assessments as an accurate and fast method in situ at the tree scale is discussed.     

Variations in parasitism in sympatric populations of three invasive leaf miners

Abstract:  Parasitism was investigated in sympatric populations of three invasive gracillariid leaf miners in Europe, Cameraria ohridella , Phyllonorycter robiniella and Phyllonorycter platani to test the hypotheses that C. ohridella is less heavily parasitized by native parasitoids and attacked by fewer species than the two other invasive species. In all regions investigated, C. ohridella showed a lower parasitism rate, and its parasitoid complex was poorer in species than those of either Phyllonorycter spp. Comparisons were made between sympatric populations of C. ohridella on its main host tree, Aesculus hippocastanum , and an occasional host, Acer pseudoplatanus . Parasitism rates were similarly low and composed of the same parasitoid species on both trees. In contrast, a sympatric population of Phyllonorycter geniculella , a native species mining A. pseudoplatanus , was heavily parasitized by a totally different parasitoid complex. These results suggest that the low parasitism in C. ohridella by native polyphagous leaf miner parasitoids is due neither to its host tree, nor to a problem of synchronization between the phenology of the pest and that of its parasitoids. Instead, it probably results from the inability of the native parasitoids to locate, attack, or develop on a new host that does not have any native congener in Europe.     

Does predation maintain tit community diversity?

European tits of the genus Parus constitute a complex group of coexisting boreal birds. Here we present a survey of the distribution of three coniferous-living Parus species and one of their main predators, the pygmy owl ( Glaucidium passerinum ), on nine isolated islands in Scandinavia. On all islands the coal tit ( Parus ater ) is the sole tit species when the pygmy owl is absent. The two larger species, the willow tit ( P. montanus ) and the crested tit ( P. cristatus ), only coexist with the coal tit when pygmy owls are present. We suggest that the coexistence of willow tits, crested tits and coal tits is the result of a combination of competition for food and predator-safe foraging sites. The smaller coal tit is superior in exploitation competition for food, while the two larger species have an advantage in interference competition for predator-safe foraging sites. The association between the distribution of the pygmy owl and the two larger tit species on isolated islands in Scandinavia is consistent with the idea that the pygmy owl is a keystone predator.     

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

Laboratory rearing and biological parameters of the eulophid Pnigalio agraules,a parasitoid of Cameraria ohridella

Predators as well as parasitoids native to Europe accept the exotic horse chestnut leafminer, Cameraria ohridella Deschka and Dimi? 1986 (Lepidoptera: Gracillariidae), either as prey or as host. However, the influence of these antagonists on the populations of the pest insect is so far very low. Therefore, efforts to develop an integrated pest management system against C. ohridella should include methods which foster the natural enemy complex. In the present study we developed a laboratory rearing method and investigated several biological parameters of Pnigalio agraules (Walker 1839) (Hymenoptera: Eulophidae), a dominant species in the horse chestnut leafminer’s parasitoid complex in many European regions. This native parasitoid satisfies three basic requirements for successful use as a biocontrol agent with regard to C. ohridella. The parasitoid’s fecundity, longevity and the speed of juvenile development by far exceeds that of the leafminer, enabling the parasitoid population to increase faster than that of the host. Furthermore, our results show that the impact of this species on C. ohridella populations has been previously underestimated, because non‐reproductive killing (i.e. host‐feeding and host‐stinging) of the hosts, resulting in considerable larval mortality of the leafminer, has not been quantitatively assessed. However, naturally occurring parasitoid populations have negligible impact on C. ohridella populations. Further studies, including experimental releases of P. agraules, are necessary to understand the constraints limiting the parasitoid’s performance in the field and to assess the potential benefits of releases for the control of C. ohridella.     

Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey

Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar‐infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.     

Aphid suppression by natural enemies in mulched cereals

Large populations of natural enemies are the basis for natural pest control. Effects of mulch on predator–prey interactions in arable fields are poorly known, despite its potential to enhance ground‐dwelling predators and thereby reduce pest infestations. We studied the densities of predators and parasitoids, and their impact on cereal aphids in the presence and absence of mulch. Released populations of the bird cherry aphid, Rhopalosiphum padi (L.) (Homoptera: Aphididae), and two naturally occurring aphid species, were monitored under experimentally reduced densities of: (i) ground‐dwelling predators, (ii) flying predators and parasitoids, and (iii) with straw mulch. The three treatments were applied in a 2 × 2 × 2 factorial design in a field of spring wheat (Triticum aestivum L.). The exclusion of ground‐dwelling predators increased aphid populations by 55% in June and 40% in July, respectively. Mulched plots had 25% lower aphid densities in June. This was presumably due to enhanced densities of spiders (Araneida) in mulched plots. The exclusion of flying predators and parasitoids led to 94% higher aphid populations in late July (109 vs. 56 individuals per 100 shoots), irrespective of mulch or ground predator manipulation. This was attributed to the larvae of gall midges Aphidoletes cf. aphidimyza (Rondani) (Diptera: Cecidomyiidae) and hoverflies (Diptera: Syrphidae). The results indicate that a scarcity of predators and a bare soil surface renders crops more susceptible to arthropod pests. Farming schemes should aim at enhancing both ground‐dwelling and flying predators for elevated levels of natural pest control.     

Experimental evidence for density dependence of reproduction in great tits

1. Density dependence of avian reproduction has often been analysed using correlations between annual mean reproductive output and population density. Experiments are necessary to prove that density is the cause of the observed patterns, but so far, three out of four experimental studies do not support a direct causal effect of density on reproduction.
2. This paper presents experimental evidence that reproductive decisions in great tits, Parus major L., are causally affected by breeding density. The breeding density of great tits was manipulated by providing nest-boxes at different densities in an ecologically homogeneous area.
3. Within years the densities in the high and low density plots differed approximately 8-fold. During the 11 years of the experiment, clutch size, nestling mass and the proportion of birds starting a second brood were all lower in the high density plot. In 5 years with equal breeding densities in both parts, clutch size did not differ between the plots. The patterns found were consistent with the density effects as predicted from the non-experimental data.