Apostolos Pekas

Energy reserves of parasitoids depend on honeydew from non-hosts

Adult parasitoids depend on sugar‐rich foods such as nectar and honeydew to meet their energy requirements and control insect pests. However, it is poorly known whether parasitoids can detect and feed on honeydew in agroecosystems, where it is the primary carbohydrate source, because this sugar source is less apparent in comparison to nectar and sometimes contains repellent compounds for parasitoids. High‐performance liquid chromatography (HPLC) analyses were carried out to test whether Aphytis melinus DeBach (Hymenoptera: Aphelinidae), a parasitoid whose host does not produce honeydew, feeds on honeydew from non‐hosts. In addition, the correlation between the parasitoids sugar reserves and honeydew abundance was determined. To do this, both the levels of honeydew producers and the sugar levels of individual collected parasitoids were assessed during different seasons. The overall sugar content was treated as an indicator of energy reserves and the erlose–melezitose ratio as an indicator of honeydew feeding. The data show that A. melinus fed commonly on honeydew from non‐host hemipterans. More than 50% of the female parasitoids collected in spring and summer had recently fed on honeydew and most of them showed a high sugar content. However, in autumn, when the number of honeydew producers was three times lower than in spring and summer, less than 20% of A. melinus were found to have fed on honeydew, with the average total sugar content being reduced by a factor of three. This study demonstrates that A. melinus commonly feeds on honeydew in the field, even though its host does not produce honeydew. The results also suggest that the exploitation of honeydew by A. melinus is a function of the density and species of honeydew producers.

Discrimination of the closely related biocontrol agents Macrolophus melanotoma (Hemiptera: Miridae) and M. pygmaeus using mitochondrial DNA analysis

The separation of the closely related predatory species Macrolophus melanotoma Costa (= M. caliginosus Wagner) and Macrolophus pygmaeus (Rambur) based exclusively on the different colour pattern of the first antennal segment (white central band in M. melanotoma and entirely black in M. pygmaeus) is rather precarious and their taxonomic status is still in doubt. In the present study their taxonomic status was evaluated by DNA confirmatory analysis and hybridization experiments between M. pygmaeus and a Macrolophus taxon, resembling M. melanotoma, with a first antennal segment entirely black or with a white central band collected from Dittrichia viscosa (L.) W. Greuter (Asteraceae) in southern Greece. Adult females from Dittrichia plants hybridized with males of M. pygmaeus and vice versa did not produce viable eggs. The Macrolophus species from Dittrichia irrespective of the first antennal segment coloration differed from M. pygmaeusin digestive patterns generated by AseI, XbaI, and MseI on 16S rRNA and in RAPD profiles produced by the primers OPA-18 and OPA-20. These results demonstrate that on Dittrichia plants there is a distinct dimorphic taxon, M. melanotoma, as it is the only species of the genus Macrolophus bearing a first antennal segment with a central white band. Given the limitation of the coloration pattern, the mtDNA genetic markers are the appropriate method for the identification of M. melanotomaand M. pygmaeus.

Effect of Mediterranean Ants (Hymenoptera: Formicidae) on California Red Scale (Hemiptera: Diaspididae) Populations in Citrus Orchards

ABSTRACT We conducted an ant-exclusion experiment in a citrus orchard to evaluate the overall impact of three ant species native in the Mediterranean, Pheidole pallidula (Nylander), Plagiolepis schmitzii Forel, and Lasius grandis (Forel), on populations of Aonidiella aurantii Maskell (California red scale). The ant-exclusion was carried out in four experimental plots from March 2007 to November 2008. Another subset of four plots, adjacent to the ant-excluded plots, was used as control. We measured scale densities and percent parasitism on fruits at harvest in 2007 and 2008. Additionally, we sampled the seasonal trend of the scale on twigs and fruits in both treatments during 2008. California red scale densities in the ant-excluded treatment began to be significantly lower than in the ant-allowed control in May (1 mo after ant activity began), and this difference increased until November. Thus, the effect of the ants on California red scale density seems to be accumulative. At harvest, scale densities on fruits were significantly lower in the ant-excluded treatment. However, percent parasitism on fruits was similar between treatments. Finally, scale densities on the fruits of the ant-allowed plots were positively correlated with the number of ants that climbed to the citrus canopy. These results suggest that increases of scale densities induced by Mediterranean ants depend on the intensity of the ant-activity on citrus canopies.

Parasitoid nutritional ecology in a community context: the importance of honeydew and implications for biological control

One focus of conservation biological control studies has been to improve the nutritional state and fitness of parasitoids by adding nectar and artificial sugars to agroecosystems. This approach has largely overlooked the presence of honeydew, which is likely the primary carbohydrate source available to parasitoids in many agroecosystems. Over the last decade, it has been demonstrated that parasitoids often utilize this sugar source and there is evidence that honeydew can indirectly impact the population dynamics of herbivores through its nutritional value for parasitoids. The consumption of honeydew by parasitoids can shape direct and indirect interactions with other arthropods. The strength of these effects will depend on: first, parasitoid biology, second, the presence of other sugar sources (mainly nectar), third, the quality and quantity of the honeydew, and fourth, the presence and competitive strength of other honeydew consumers such as ants. The combination of these four factors is expected to result in distinct scenarios that should be analyzed for each agroecosystem. This analysis can reveal opportunities to increase the biocontrol services provided by parasitoids. Moreover, honeydew can be a resource-rich habitat for insect pathogens; or contain plant secondary chemicals sequestered by hemipterans or systemic insecticides toxic for the parasitoid. Their presence and effect on parasitoid fitness will need to be addressed in future research.

Comparison of bacterial microbiota of the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and its factitious prey Tyrophagus putrescentiae (Acari: Acaridae)

Neoseiulus cucumeris is a predatory mite used for biological control of arthropod pests. Mass-reared predators are fed with factitious prey mites such as Tyrophagus putrescentiae. Although some information on certain endosymbionts of N. cucumeris and T. putrescentiae exists, it is unclear whether both species share bacterial communities. The bacterial communities in populations of predator and prey mites, as well as the occurence of potential acaropathogenic bacteria were analyzed. The comparisons were based on the following groups: (i) N. cucumeris mass-production; (ii) N. cucumeris laboratory population with disease symptoms; (iii) T. putrescentiae pure populations and; (iv) T. putrescentiae from rearing units of N. cucumeris. Only 15% of OTUs were present in all samples from predatory and prey mite populations (core OTUs): the intracellular symbionts Wolbachia, Cardinium, plus other Blattabacterium-like, Solitalea-like, and Bartonella-like symbionts. Environmental bacteria were more abundant in predatory mites, while symbiotic bacteria prevailed in prey mites. Relative numbers of certain bacterial taxa were significantly different between the microbiota of prey mites reared with and without N. cucumeris. No significant differences were found in the bacterial communities of healthy N. cucumeris compared to N. cucumeris showing disease symptoms. We did not identify any confirmed acaropathogenic bacteria among microbiota.

Host size and spatiotemporal patterns mediate the coexistence of specialist parasitoids

Many insect parasitoids are highly specialized and thus develop on only one or a few related host species, yet some hosts are attacked by many different parasitoid species in nature. For this reason, they have been often used to examine the consequences of competitive interactions. Hosts represent limited resources for larval parasitoid development and thus one competitor usually excludes all others. Although parasitoid competition has been debated and studied over the past several decades, understanding the factors that allow for coexistence among species sharing the same host in the field remains elusive. Parasitoids may be able to coexist on the same host species if they partition host resources according to size, age, or stage, or if their dynamics vary at spatial and temporal scales. One area that has thus far received little experimental attention is if competition can alter host usage strategies in parasitoids that in the absence of competitors attack hosts of the same size in the field. Here, we test this hypothesis with two parasitoid species in the genus Aphytis, both of which are specialized on the citrus pest California red scale Aonidiella aurantii. These parasitoids prefer large scales as hosts and yet coexist in sympatry in eastern parts of Spain. Parasitoids and hosts were sampled in 12 replicated orange groves. When host exploitation by the stronger competitor, A. melinus, was high the poorer competitor, A. chrysomphali, changed its foraging strategy to prefer alternative plant substrates where it parasitized hosts of smaller size. Consequently, the inferior parasitoid species shifted both its habitat and host size as a result of competition. Our results suggest that density-dependent size-mediated asymmetric competition is the likely mechanism allowing for the coexistence of these two species, and that the use of suboptimal (small) hosts can be advantageous under conditions imposed by competition where survival in higher quality larger hosts may be greatly reduced.

Ants impact the energy reserves of natural enemies through the shared honeydew exploitation

1. Ants, as well as many species of parasitoids and predators, rely on sugar‐rich foods such as honeydew to fulfill their energetic needs. Thus, ants and natural enemies may interact through the shared honeydew exploitation.

Ants affect the infestation levels but not the parasitism of honeydew and non-honeydew producing pests in citrus

Ants act simultaneously as predators and as hemipteran mutualists, and thereby may affect the composition and population dynamics of a wide arthropod community. We conducted ant-exclusion experiments in order to determine the impact of ants on the infestation levels and parasitism of three of the most important citrus pests of western Mediterranean citrus: the honeydew producer Aleurothrixus floccosus Maskell (woolly whitefly) and the non-honeydew producers Aonidiella aurantii Maskell (California red scale; CRS) and Phyllocnistis citrella (Staiton) (citrus leafminer). The study was conducted in three commercial citrus orchards, each one dominated by one ant species (Pheidole pallidula, Lasius grandis or Linepithema humile) during two consecutive growing seasons (2011 and 2012). We registered a significant reduction of the CRS densities on fruits in the ant-excluded treatment in the three orchards and in the two seasons, ranging from as high as 41% to as low as 21%. Similarly, the percentage of shoots occupied by A. floccosus was significantly lower in the ant-excluded plots in the orchards dominated by P. pallidula and L. humile. No significant differences were registered in the percentage of leaf surface loss caused by P. citrella between ant-allowed and ant-excluded treatments in any case. We found no significant differences in the percent parasitism between ant-allowed and ant-excluded treatments for honeydew and non-honeydew producing herbivores. These results suggest that: (i) ant management should be considered in order to reduce herbivore populations in citrus and (ii) mechanisms other than parasitism (e.g., predation) might explain the differences in herbivore infestation levels between treatments.

Non-target effects of commonly used plant protection products in roses on the predatory mite Euseius gallicus Kreiter & Tixier (Acari: Phytoseidae)

BACKGROUND Euseius gallicus Kreiter & Tixier (Acari: Phytoseidae) is a predatory mite recently available for use against various pests in roses. We tested in greenhouse trials the impact on the numbers of eggs and motiles of E. gallicus of the most commonly used plant protection products in roses in northern Europe: the acaricides acequinocyl and etoxazole, the insecticides azadirachtin-A, acetamiprid, flonicamid, imidacloprid, indoxacarb, thiacloprid and thiamethoxam and the fungicides boscalid and kresoxim-methyl, cyprodinil + fludioxonil, dodemorph and fluopyram + tebuconazole. RESULTS The neonicotinoids thiacloprid, thiamethoxam, acetamiprid and imidacloprid had a negative impact on the number of eggs (47, 62, 81 and 76% reduction, respectively, compared with a water treatment) and number of motiles of E. gallicus (42.2, 42.9, 59.9 and 60.6% reduction) and were classified as slightly to moderately toxic. Also, the number of motiles was reduced after treatment with acequinocyl (47%) and etoxazole (43.9%) and after two treatments with flonicamid (41%) with a 1 week interval between treatments. CONCLUSION Azadirachtin-A, acetamiprid, flonicamid, boscalid and kresoxim-methyl, cyprodinil + fludioxonil, dodemorph and fluopyram + tebuconazole were harmless for E. gallicus. Special attention should be paid to the impact of neonicotinoids and of acequinocyl and etoxazole, and to the application frequency with flonicamid on E. gallicus.

Multiple resource supplements synergistically enhance predatory mite populations

Many plants offer food rewards such as extrafloral nectar and food bodies, which have been shown to attract and retain entomophagous arthropods. In addition to food rewards, plants may possess structures that serve as shelter and/or oviposition sites for beneficial arthropods, so-called domatia. Acarodomatia are commonly used by beneficial mites for oviposition and protection from intraguild predators and adverse climatic conditions (drought). While in nature these food and shelter traits often occur in combination, they have been largely studied in isolation and we know little about how these traits interact, i.e., whether they act independently, antagonistically or synergistically. In the present study, we used citrus seedlings to test the impact of provisioning fibers (as a proxy for acarodomatia), as well as two different categories of food rewards (pollen and sugars) on oviposition and population development of phytoseiid mites. The highest oviposition and abundance of predatory mites was obtained in the treatment where the three resources were offered in combination. The combined impact of the three resources when provided jointly was up to five times higher than the summed impacts of each resource provided individually, thus providing evidence for a three-way synergy between the fibers, pollen and sugars. From an ecological point of view, our results demonstrate that combining multiple indirect defensive traits can strongly enhance the impact on the mutualistic arthropods. Differences in resource provisioning strategies in plant–phytoseiid and plant–ant mutualisms are being discussed. The presented results are of particular importance for our understanding of the functioning of defensive plant-arthropod mutualisms, as well as for the use of predatory mites in conservation- or inundative biological control.