'Divergent male ontogenies' in Aphelinidae (Hymenoptera: Ghalcidoidea): a simplified classification and a suggested evolutionary sequence

A classification of the different types of divergent male ontogeny in Aphelinidae is proposed to replace the little known and cumbersome systems previously published. All the Aphelinidae in which conspecific males and females have different host relationships, i.e. those that have divergent ontogenies, are here designated heteronomous parasitoids. Females of these species are primary endoparasitoids of Homoptera. The males of (i) diphagous parasitoids are primary ectoparasitoids of the same host species exploited by their females, (ii) heteronomous hyperparasitoids develop hyperparasitically, and (iii) heterotrophic species are endoparasitoids of lepidopterous eggs. Heteronomous hyperparasitoids can be classified further as obligate autoparasitoids, facultative autoparasitoids or alloparasitoids. All the species of heteronomous aphelinids whose biologies are known are listed according to the new classification, and the evolutionary sequence of these unusual host relationships is discussed.     

The impact of an ant–aphid mutualism on the functional composition of the secondary parasitoid community

1. Mutualistic and antagonistic interactions, although often studied independently, may affect each other, and food web dynamics are likely to be determined by the two processes working in concert. 2. The structure, and hence dynamics, of food webs depends on the relative abundances of generalist and specialist feeding guilds. Secondary parasitoids of aphids can be divided into two feeding guilds: (i) the more specialised endoparasitoids, which attack the primary parasitoid larvae in the still living aphid, and (ii) the generalist ectoparasitoids, which attack the pre‐pupa of the primary or secondary parasitoid in the mummified aphid. 3. We studied the effect of an ant–aphid mutualism on the relative abundance of these two functional groups of secondary parasitoids. We hypothesised that generalists will be negatively affected by the presence of ants, thus leading to a greater dominance of specialists. 4. We manipulated the access of ants (Lasius niger) to aphid colonies in which we placed parasitised aphids. Aphid mummies were collected and reared to determine the levels of endo‐ and ecto‐secondary parasitism. 5. When aphids were attended by L. niger the proportion of secondary parasitism by ectoparasitoids dropped from 26 to 8% of the total number of parasitised aphids, with Pachyneuron aphidis most strongly affected, while endoparasitoids as a group did not respond. However, among these Syrphophagus mamitus profited from ant attendance becoming the dominant secondary parasitoid, while parasitisation rates of Alloxysta and Phaenoglyphis declined. 6. The shift to S. mamitus as dominant secondary parasitoid in ant‐attended aphid colonies is likely due to the behavioural plasticity of this species in response to ant aggression, and a release from tertiary parasitism by generalist ectoparasitoids. 7. The reduction of secondary parasitism by generalist ectoparasitoids reduces the potential for apparent competition among primary parasitoids with consequences for the dynamics of the wider food web.     

Trophic assimilation efficiency markedly increases at higher trophic levels in four-level host–parasitoid food chain

Trophic assimilation efficiency (conversion of resource biomass into consumer biomass) is thought to be a limiting factor for food chain length in natural communities. In host–parasitoid systems, which account for the majority of terrestrial consumer interactions, a high trophic assimilation efficiency may be expected at higher trophic levels because of the close match of resource composition of host tissue and the consumer''s resource requirements, which would allow for longer food chains. We measured efficiency of biomass transfer along an aphid-primary–secondary–tertiary parasitoid food chain and used stable isotope analysis to confirm trophic levels. We show high efficiency in biomass transfer along the food chain. From the third to the fourth trophic level, the proportion of host biomass transferred was 45%, 65% and 73%, respectively, for three secondary parasitoid species. For two parasitoid species that can act at the fourth and fifth trophic levels, we show markedly increased trophic assimilation efficiencies at the higher trophic level, which increased from 45 to 63% and 73 to 93%, respectively. In common with other food chains, δ¹⁵N increased with trophic level, with trophic discrimination factors (Δ¹⁵N) 1.34 and 1.49‰ from primary parasitoids to endoparasitic and ectoparasitic secondary parasitoids, respectively, and 0.78‰ from secondary to tertiary parasitoids. Owing to the extraordinarily high efficiency of hyperparasitoids, cryptic higher trophic levels may exist in host–parasitoid communities, which could alter our understanding of the dynamics and drivers of community structure of these important systems.     

Natural enemies ofPlutella xylostella (Lep.: Plutellidae) on crucifers in Honduras

Three primary parasitoids in three genera were reared fromPlutella xylostella (L.) larvae and pupae collected in various crucifer producing regions of Honduras. The ichneumonidDiadegma insulare (Cresson) was by far the most abundant species. TwoSpilochalcis species, facultative hyperparasitoids attackingP. xylostella andD. insulare, were encountered as well as eleven species in nine genera of obligate hyperparasitoids attackingD. insulare. Three vespid predators are noted as predating on larvae.      

Interspecific and nutrient-dependent variations in stable isotope fractionation: experimental studies simulating pelagic multitrophic systems

Stable isotope signatures of primary producers display high inter- and intraspecific variation. This is assigned to species-specific differences in isotope fractionation and variable abiotic conditions, e.g., temperature, and nutrient and light availability. As consumers reflect the isotopic signature of their food source, such variations have direct impacts on the ecological interpretation of stable isotope data. To elucidate the variability of isotope fractionation at the primary producer level and the transfer of the signal through food webs, we used a standardised marine tri-trophic system in which the primary producers were manipulated while the two consumer levels were kept constant. These manipulations were (1) different algal species grown under identical conditions to address interspecific variability and (2) a single algal species cultivated under different nutrient regimes to address nutrient-dependent variability. Our experiments resulted in strong interspecific variation between different algal species (Thalassiosira weissflogii, Dunaliella salina, and Rhodomonas salina) and nutrient-dependent shifts in stable isotope signatures in response to nutrient limitation of R. salina. The trophic enrichment in ¹⁵N and ¹³C of primary and secondary consumers (nauplii of Acartia tonsa and larval herring) showed strong deviations from the postulated degree of 1.0‰ enrichment in δ¹³C and 3.4‰ enrichment in δ¹⁵N. Surprisingly, nauplii of A. tonsa tended to keep “isotopic homeostasis” in terms of δ¹⁵N, a pattern not described in the literature so far. Our results suggest that the diets’ nutritional composition and food quality as well as the stoichiometric needs of consumers significantly affect the degree of trophic enrichment and that these mechanisms must be considered in ecological studies, especially when lower trophic levels, where variability is highest, are concerned.     

Effects of environmental stress cascade up through four trophic levels in a salt marsh study system

1. Although in recent years there have been a number of studies demonstrating trophic cascades in terrestrial systems, it is still unclear what environmental conditions enable or enhance such cascades, especially among four trophic levels. 2. In this study, the influence of environmental stress (increased soil pore water salinity) on a four trophic level study system in a Florida salt marsh was examined by experimentally increasing soil pore water salinity. Effects of increased salinity on the quality of the host plant, Batis maritima, were assessed, as were resulting effects on the lepidopteran herbivore Ascia monuste, and the primary parasitoids and hyperparasitoids of its caterpillars. 3. Increased salinity altered host‐plant quality, which subsequently affected the consumer species. These effects of altered plant quality cascaded up through the herbivore and primary parasitoid to the hyperparasitoid Hypopteromalus inimicus, influencing its density, sex ratio, body size, and initial egg load. 4. These results demonstrate how heterogeneity in environmental stress can result in effects that cascade up through four trophic levels. We suggest that such strong effects at higher trophic levels may be more likely in systems in which relationships are more specific and intimate such as those among hosts, parasitoids, and hyperparasitoids.     

Production of yeastolates for uniform stable isotope labelling in eukaryotic cell culture

Preparation of stable isotope-labelled yeastolates opens up ways to establish more cost-effective stable isotope labelling of biomolecules in insect and mammalian cell lines and hence to employ higher eukaryotic cell lines for stable isotope labelling of complex recombinant proteins. Therefore, we evaluated several common yeast strains of the Saccharomycetoideae family as a source of high-quality, non-toxic yeastolates with the major aim to find a primary amino acid source for insect and mammalian cell culture that would allow cost-effective uniform stable isotope labelling (¹³C, ¹⁵N). Strains of the facultative methylotrophic yeasts Pichia pastoris and Hansenula polymorpha (Pichia angusta) as well as a strain of the baker’s yeast Saccharomyces cerevisiae were compared as a source of yeastolate with respect to processing, recovery and ability to sustain growth of insect and mammalian cell lines. The best growth-supporting yeastolates were prepared via autolysis from yeast obtained from fed-batch cultures that were terminated at the end of the logarithmic growth phase. Yeastolates obtained from H. polymorpha performed well as a component of insect cell cultures, while yeastolates from S. cerevisiae and H. polymorpha both yielded good results in mammalian cell cultures. Growth of yeasts in Heine’s medium without lactic acid allows relatively low concentrations of ¹³C and ¹⁵N sources, and this medium can be reused several times with supplementation of the ¹³C source only.     

Parasitoids associated with the common pistachio psylla, Agonoscena pistaciae, in Iran

The parasitoids associated with the common pistachio psylla, Agonoscena pistaciae Burckhardt and Lauterer, were investigated at three pistachio plantations in Rafsanjan, Iran. Of the 6504 wasps emerging from mummified psyllids, 46% were the primary parasitoid Psyllaephagus pistaciae Ferrière, and the remaining 54% represented six species of hymenopterous hyperparasitoids, including Chartocerus kurdjumovi (Nikol’skaja), Marietta picta (André), Pachyneuron aphidis (Bouché), Pachyneuron muscarum (Linnaeus), Psyllaphycus diaphorinae (Hayat), and Syrphophagus aphidivorus (Mayr). Lysiphlebus fabarum Marshall, the parasitoid of Aphis gossypii Glover and Aphis craccivora Koch present on weeds, was found to be an alternative host for three major hyperparasitoids of A. pistaciae. The most abundant hyperparasitoid was S. aphidivorus, appearing during the growing season in all trial locations on psyllids and aphids in pistachio orchards. The weed-infesting aphids, along with their primary parasitoid, can act as a reservoir of A. pistaciae secondary parasitoids. Therefore, parasitized aphids allow populations of secondary parasitoids to increase and consequently to apply higher pressure on P. pistaciae. We detected that two primary parasitoid species, including P. pistaciae and L. fabarum, attacking different species of hosts interact indirectly through shared secondary parasitism. It is suggested that the community structure of A. pistaciae may be influenced by apparent competition, although more work is needed to provide firm evidence.     

Stable isotopes and trophic positions of littoral fishes from a Mediterranean marine protected area

Stable isotope analyses were employed to explore feeding and foraging habitats and trophic levels of littoral fishes in a western Mediterranean Marine Protected Area (Egadi Islands, Sicily, Italy). Carbon and nitrogen stable isotope ratios were measured in primary producers, invertebrates and fishes collected in December 2001 and January 2002. Fishes of the littoral region of the Egadi Islands had isotopic signatures that fell into a wider range for δ ¹³C (about 6‰) than for δ ¹⁵N (about 3‰). Carbon isotope ratios were consistent with a food web based on mixed sources and two trophic pathways leading to different fish species. Differences in the isotopic composition between islands were higher for benthivorous than for planktivorous fishes. The overall picture gained from this study is of a isotopic distinction between planktivorous and benthivorous fishes, resource partitioning facilitating the coexistence of similar species within the same ecosystem, and spatial variability in the isotopic signatures and trophic level of fishes. Asymmetrical analysis of variance showed that estimated trophic levels were lower in the area with the highest level of protection (Zone A) for only two out of the nine fishes analysed. As a consequence, overall spatial differences do not seem to be a consequence of protection, since in most cases trophic levels did not change significantly between zone A and zones C where professional fishing (trawling apart) is permitted, but of natural sources of variation (e.g. variability in food availability and site-specific food preferences of fishes). However, the results of this study suggest a different response at the species compared to the community level.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Preliminary assessment of Greenland halibut diet in Cumberland Sound using stable isotopes

We provide preliminary carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope assessment of the Greenland halibut (Reinhardtius hippoglossoides) diet in Cumberland Sound, with focus on two possible prey sources: pelagic represented by capelin (Mallotus villosus) and epibenthic represented by shrimp (Lebbeus polaris). The δ¹³C for the Greenland halibut stock indicated a pelagic carbon source in Cumberland Sound while stable isotope mixing models, IsoSource and MixSIR, indicated a 99% dietary composition of capelin relative to the shrimp. The δ¹⁵N did not vary across Greenland halibut size ranges and placed them at a fourth trophic position relative to a primary herbivore. This study provides the starting point for more elaborate Cumberland Sound research on the local Greenland halibut feeding ecology by confirming pelagic feeding and establishing relative trophic position as well as identifying stable isotopes as a useful tool for the study of diet in cold water fish species.     

Changes in trophic linkages to shortfin eels (<Emphasis Type="Italic">Anguilla australis</Emphasis>) since the collapse of submerged macrophytes in Lake Ellesmere,New Zealand

Lake Ellesmere (Te Waihora) is a nationally important coastal brackish lake in New Zealand, however degradation in water quality and loss of submerged macrophytes over past decades have raised concerns in regards to the declining status of the lake’s commercial and customary fisheries, predominantly targeted at shortfin eels (Anguilla australis). We investigated foodweb dynamics and trophic linkages to shortfin eels in Lake Ellesmere using a combination of abundance assessments, dietary studies, and stable isotope analyses. Data from our study are compared with historical data sets on benthic invertebrate community composition and shortfin eel diets to trace changes in the trophic linkages to top predators that have occurred since the late 1960s. Stable isotope analyses indicate that the foodweb is predominantly driven by epipelic and phytoplankton derived carbon sources, although it was difficult to discriminate between these two carbon pools because of wind-driven resuspension of lake sediments. Comparison of our survey results with historical data sets indicates a clear shift in benthic biota from being dominated by phytofaunal species such as Potamopyrgus antipodarum (comprising 90% of total invertebrate biomass) during the 1960s, to now being almost entirely comprised of subterranean species such as Chironomus zealandicus and oligochaetes (together comprising 82% of total invertebrate biomass). This shift in benthic communities has resulted in significant changes in the size-specific diet of juvenile shortfin eels (<400 mm) from those reported for Lake Ellesmere during the mid 1970s, with Chironomus larvae now comprising 65% of the diets of juvenile eels, whereas historically P. antipodarum was the dominant food item (>30% of total biomass). This shift towards foraging on smaller sediment-dwelling species could have implications for juvenile eel bioenergetics, and may help explain why juvenile shortfin growth rates have significantly decreased in past decades. Juvenile shortfins now appear to switch to foraging on preyfish (mainly common bullies, Gobiomorphus cotidianus) at a smaller size (≈400 mm) than historically recorded (>500 mm). Dietary and stable isotope signatures indicated that small shortfins (100–299 mm) have considerable overlap in trophic position (δ¹³C = −20.4‰, δ¹⁵N = 13.6‰) with common bullies (δ¹³C = −20.5‰, δ¹⁵N = 13.7‰), the dominant fish in Lake Ellesmere (92% of total abundance CPUE), potentially indicating that these two species may directly compete for food resources. These findings again highlighted the importance of C. zealandicus in sustaining the fish populations of the lake. Handling editor: S. Declerck     

Host Location and Ovipositional Behavior of Platygaster demades Walker (Hymenoptera: Platygastridae), an Egg Parasitoid of Apple and Pear Leaf Curling Midges

The foraging responses of 1–2-day-old naïve female Platygaster demades to odors of apple and pear foliage and host insect eggs were measured. The host origin of P. demades had no effect on the parasitoids’ longevity, host preference, or foraging behavior. Four distinct behaviors related to oviposition were identified. In choice experiments, more female parasitoids responded to apple foliage with no midge eggs than to midge eggs alone. In a Y-tube olfactometer, parasitoids preferred the plant cues to clean air, and responded equally to both apple and pear odors. The results indicate that P. demades utilizes plant cues to locate the habitat of its host and then searches for host eggs to parasitize.     

Piscivorous birds as top predators and fishery competitors in the lagoon ecosystem

Trophic patterns of omnivorous freshwater shrimps, Exopalaemon modestus and Macrobrachium nipponensis, were investigated in two shallow eutrophic lakes by using stable isotope analysis. δ¹⁵N and δ¹³C of M. nipponensis and E. modestus increased with increasing body weight, which might be attributed to larger individuals ingesting organisms that feed higher up the food chain and/or increased assimilation of benthic food items with enriched isotopic signatures. Of the freshwater shrimps occurring in the studied lakes, those from Lake Taihu had significantly elevated δ¹⁵N and δ¹³C values (4.3‰ and 1.8‰, respectively) compared with those from the less eutrophic Lake Chaohu, indicating that the isotopic signature might partially reflect the trophic states of their habitats. Mixing model results suggested that the benthic food web provides the primary carbon source for both shrimp species, and that E. modestus assimilated relatively more pelagic food sources than M. nipponensis in these lakes. Handling editor: S. Wellekens     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

Isotopic enrichment in herbivorous insects: a comparative field-based study of variation

Researchers will be able to use stable isotope analysis to study community structure in an efficient way, without a need for extensive calibrations, if isotopic enrichment values are consistent, or if variation in enrichment values can be predicted. In this study, we generated an experimental data set of δ¹⁵N and δ¹³C enrichment means for 22 terrestrial herbivorous arthropods feeding on 18 different host plants. Mean enrichments observed across a single trophic transfer (plants to herbivores) were −0.53±0.26‰ for δ¹³C (range: −3.47‰ to 1.89‰) and 1.88±0.37‰ for δ¹⁵N (range: −0.20‰ to 6.59‰). The mean δ¹³C enrichment was significantly lower than that reported in recent literature surveys, whereas the mean δ¹⁵N enrichment was not significantly different. The experimental data set provided no support for recent hypotheses advanced to explain variation in enrichment values, including the proposed roles for consumer feeding mode, development type, and diet C:N ratio. A larger data set, formed by combining our experimental data with data from the literature, did suggest possible roles for feeding mode, nitrogen recycling, herbivore life stage, and host plant type. Our results indicate that species enrichment values are variable even in this relatively narrow defined group of organisms and that our ability to predict enrichment values of terrestrial herbivorous arthropods based on physiological, ecological, or taxonomic traits is low. The primary implications are that (1) mean enrichment may have to be measured empirically for each trophic link of interest, rather than relying on estimates from a broad survey of animal taxa and (2) the advantage of using stable isotope analysis to probe animal communities that are recalcitrant to other modes of study will be somewhat diminished as a consequence.Electronic Supplementary Material Supplementary material is available for this article at     

Parasitoid complex of the pistachio twig borer moth,Kermania pistaciella,in Iran

The parasitoid complex of the pistachio twig borer moth, Kermania pistaciella Amsel (Lepidoptera: Tineidae), a native pest of pistachio trees, was investigated at 27 pistachio plantation sites in Kerman province, the major pistachio growing area of Iran. The present study was conducted to document the naturally established parasitoid complex and to assess the need for improving the biological control of this species. In total, 22,390 moth cocoons were collected from 186 samples collected from commercial orchards during 2006–2008 and kept singly in controlled conditions to rear immature insects. An average of 2.8% of moth cocoons had been attacked by predators at time of sampling. Of the collected cocoons, on average 46.7% completed development and emerged as adult moths, no insects emerged from 8%, suggesting that the moth or wasp died before maturing, and parasitoids emerged from the remaining 42.5%. The overall percentage of host cocoons from which wasps emerged ranged from 25.6 to 59%. Fifteen hymenopterous parasitoid species were recovered from cocoons, of which three species were primary parasitoids, two were obligatory hyperparasitoids and the remaining 10 species were facultative hyperparasitoids. The primary parasitoid, Chelonus kermakiae (Tobias) (Hymenoptera: Braconidae), was the most abundant comprising almost 85% of the total emerging parasitoids. In addition, a further four species of larval parasitoid developed within the PTBM's larval tunnels in pistachio fruit cluster-stem tissue. Conservation of these parasitoids in the pistachio growing areas is recommended since a high level of parasitized moths’ cocoons was found at the majority of experimental sites.     

The trophic structure of bark-living oribatid mite communities analysed with stable isotopes (15N, 13C) indicates strong niche differentiation

The aim of the present study was to identify food sources of bark-living oribatid mites to investigate if trophic niche differentiation contributes to the diversity of bark living Oribatida. We measured the natural variation in stable isotope ratios (¹⁵N/¹⁴N, ¹³C/¹²C) in oribatid mites from the bark of oak (Quercus robur), beech (Fagus sylvatica), spruce (Picea abies) and pine (Pinus sylvestris) trees and their potential food sources, i.e., the covering vegetation of the bark (bryophytes, lichens, algae, fungi). As a baseline for calibration the stable isotope signatures of the bark of the four tree species were measured and set to zero. Oribatid mite stable isotope ratios spanned over a range of about 13 δ units for ¹⁵N and about 7 δ units for ¹³C suggesting that they span over about three trophic levels. Different stable isotope signatures indicate that bark living oribatid mites feed on different food sources, i.e., occupy distinct trophic niches. After calibration stable isotope signatures of respective oribatid mite species of the four tree species were similar indicating close association of oribatid mites with the corticolous cover as food source. Overall, the results support the hypothesis that trophic niche differentiation of bark living oribatid mites contributes to the high diversity of the group.     

Intrinsic competition between primary hyperparasitoids of the solitary endoparasitoid Cotesia rubecula

1. In nature, competitive interactions occur when different species exploit similar niches. Parasitic wasps (parasitoids) often have narrow host ranges and need to cope with competitors that use the same host species for development of their offspring. When larvae of different parasitoid species develop in the same host, this leads to intrinsic and often contest competition. Thus far, most studies on intrinsic competition have focused on primary parasitoids. However, competition among primary hyperparasitoids, parasitic wasps that use primary parasitoids as a host, has been little studied. 2. This study investigated intrinsic competition between two primary hyperparasitoids, the gregarious Baryscapus galactopus and the solitary Mesochorus gemellus, which lay their eggs in primary parasitoid larvae of Cotesia rubecula, while those in turn are developing inside their herbivore host, Pieris rapae. The aims were to identify: (i) which hyperparasitoid is the superior competitor; and (ii) whether oviposition sequence affects the outcome of intrinsic competition. 3. The results show that B. galactopus won 70% of contests when the two hyperparasitoids parasitised the host at the same time, and 90% when B. galactopus oviposited first. When M. gemellus had a 48 h head start, the two hyperparasitoids had an equal chance to win the competition. This suggests that B. galactopus is an intrinsically superior competitor to M. gemellus. Moreover, the outcome of competition is affected by time lags in oviposition events. 4. In contrast to what has been reported for primary parasitoids, we found that a gregarious hyperparasitoid species had a competitive advantage over a solitary species.     

Molecular Markers for Identification of the Hyperparasitoids Dendrocerus carpenteri and Alloxysta xanthopsis in Lysiphlebus testaceipes Parasitizing Cereal Aphids

Polymerase chain reaction (PCR)-based molecular markers have been developed to detect the presence of primary parasitoids in cereal aphids and used to estimate primary parasitism rates. However, the presence of secondary parasitoids (hyperparasitoids) may lead to underestimates of primary parasitism rates based on PCR markers. This is because even though they kill the primary parasitoid, it’s DNA can still be amplified, leading to an erroneous interpretation of a positive result. Another issue with secondary parasitoids is that adults are extremely difficult to identify using morphological characters. Therefore, we developed species-specific molecular markers to detect hyperparasitoids. A 16S ribosomal RNA mitochondrial gene fragment was amplified by PCR and sequenced from two secondary parasitoid species, Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae) and Alloxysta xanthopsis (Ashmead) (Hymenoptera: Charipidae), four geographic isolates of the primary parasitoid, Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae), and six aphid species common to cereal crops. Species-specific PCR primers were designed for each insect on the basis of these 16S rRNA gene sequences. Amplification of template DNA, followed by agarose gel electrophoresis, successfully distinguished D. carpenteri and A. xanthopsis from all four isolates of L. testaceipes and all six cereal aphid species in this laboratory test.