Optimized timing of parasitoid release: a mathematical model for biological control of <Emphasis Type="Italic">Drosophila suzukii</Emphasis>

We present a model for the population dynamics of the invasive fruit fly Drosophila suzukii and its pupal parasitoid Trichopria drosophilae. Seasonality of the environment is captured through a system of delay differential equations with variable delays. The model is used to explore optimal timing for releasing parasitoids in biological control programs. According to the results, releasing parasitoids is most effective between late spring and early summer when the host population begins to increase. A single parasitoid release event can be more efficient than multiple releases over a prolonged period, but multiple releases are more robust to suboptimal timing choices. The findings can be useful for optimizing parasitoid release and should be transferable for similar systems. More generally, the model is an example for stage-structured resource-consumer dynamics in a varying environment.     

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.     

Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure

In this study we examined the influences that differing life history strategies and population structures at the time of pesticide exposure have on population susceptibility to pesticides. We used life table data and a matrix projection model to incorporate combinations of mortality (lethal effect) and reductions in fecundity (sublethal effect) into estimates of intrinsic population growth rates (r) for a predator, the seven-spot lady beetle, Coccinella septempunctata L., and its prey, the pea aphid, Acyrthosiphon pisum Harris, and an aphid parasitoid, Diaeretiella rapae (M’Intosh). All three species exhibited differences in key life history variables. The aphid had the highest r and shortest generation time, the ladybeetle had the lowest r and longest generation, while the parasitoid exhibited intermediate life history characteristics. When the model was run with populations started as neonates (aphids) or eggs (lady beetle, parasitoid) for each species, ladybeetle populations were much more susceptible than either aphid or parasitoid populations 30 days after simulated exposure to a pesticide. For example, 50% mortality and a 50% reduction in fecundity resulted in a population headed toward extinction (negative r) for the ladybeetle while the parasitoid population grew exponentially (positive r) even after sustaining 70% mortality and a 70% reduction in fecundity. The aphid species maintained exponential growth after sustaining 80% mortality and an 80% reduction in fecundity. Thus, differences in life history variables accounted for the greater susceptibility of the ladybeetle to a pesticide than its aphid prey or the parasitoid over a set time interval. These differences in susceptibility were greatly reduced when the model was run starting with a mixed age/stage population (the stable age distribution) for each species indicating that population structure at the time of pesticide exposure plays a critical role in population susceptibility. These results suggest that life history attributes as well as population structure at the time of pesticide exposure both play a major role in population susceptibility to pesticides, highlighting the need to explicitly consider differences in life history variables among species when calculating compatibility of pesticides and biological control agents as well as the population structure of beneficial species at the time of pesticide application.     

The Endosymbiont Arsenophonus Is Widespread in Soybean Aphid,Aphis glycines,but Does Not Provide Protection from Parasitoids or a Fungal Pathogen

Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.     

Perspective of practical biological control and population theories

We have not yet had sufficient theoretical explanation for successful biological control in which a key pest is controlled after an introduction of natural enemies. I compare here real features of successful biological control and theoretical host–parasitoid population models to reduce the gap between theory and practice. I first review the historical interaction between classical biological control projects and theoretical population models. Second, I consider the importance of host refuges in host–parasitoid population dynamics as concerns the mechanisms of low and stable host density. The importance of density–dependent parasitism through parasitoid reproduction in multivoltine host–parasitoid systems and supplemental generalist natural enemies are also discussed. Finally, I consider the difference in tactics for classical biological control and for augmentation of natural enemies in annual crop systems. Received: December 20, 1998 / Accepted: January 15, 1999     

The effect of banker plant species on the fitness of Aphidius colemani Viereck and its aphid host (Rhopalosiphum padi L.)

Banker plants, a type of open-rearing unit, are increasingly used in greenhouse crops to sustain natural enemy populations at times of low pest abundance. The most common banker plant system is a non-crop, cereal plant which supports Rhopalosiphum padi L. as an alternative host for Aphidius colemani Viereck. Although bottom-up effects of plants are known to affect natural enemies, this aspect has generally been ignored in previous investigations of banker plant efficacy. Here, we tested four cereal plant species with three varieties each to investigate host plant effects on R. padi and A. colemani. Though limited differences were observed in laboratory experiments spanning one aphid or parasitoid generation, longer greenhouse experiments spanning several generations revealed significant plant effects on both insects. R. padi performed poorly on oats (Avena sativa L.), resulting in wasps with the longest female development time, lowest emergence rates, and the lowest number of wasps produced per unit. Rye (Secale cereal L.) – intermediate in terms of aphid performance – produced a significantly male-biased wasp population with the smallest males. Conversely, R. padi placed onto either wheat (Triticum aestivum L.) or barley (Hordeum vulgare L.) performed consistently well in terms of aphid and parasitoid fitness and abundance, though neither species was obviously superior over the other. Overall, cultivars within each plant species did not significantly affect outcomes. As each plant species tested had different positive effects on aphid and parasitoid phenotypes, the potential benefits of mixing of cereal species is an area for future investigation.     

Efficacy of the parasitoid,Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) against Myzus persicae (Sulzer) (Hemiptera: Aphididae) infesting rapeseed-mustard

Efficacy of Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) was determined by studying its biological and behavioural attributes on the aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Total developmental duration of the parasitoid was longer in younger instars compared to that in older instars of aphid. Host age negatively affected the oviposition period and fecundity of the ovipositing parasitoid. Survival of the immatures was higher in older than the younger instars of the aphid. Sex ratio for the parasitoid was female-biased. Longevity of female parasitoid was higher while parasitizing aphid nymphs of younger age groups (1–2 days old) compared to that of older age groups (4–5 days old). Parasitoid showed a higher preference towards second instar of M. persicae both in choice and no-choice tests. Results on mutual interference revealed that per capita searching efficiency decreased from 0.91 to 0.07 as parasitoid densities increased from 1 to 8. Logistic regression exhibited a type II functional response for D. rapae. The estimated values of search-efficiency (a) and handling time (T_h) were 0.038 h⁻¹ and 1.59 h, respectively. The maximum parasitization rate was 15.08. This investigation suggests that D. rapae could be an effective candidate for augmentative biological control of M. persicae which infests several plant species of economic importance.     

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.     

Autumn, winter and spring dynamics of aphid Sitobion avenae and parasitoid Aphidius rhopalosiphi interactions

The potential of parasitoids for aphid control during summer has been well documented. Few results are available on the impact of parasitoid populations on aphid hosts during autumn and winter and on the dynamics of their interactions during this period. The population development of Sitobion avenae, in Belgium, is analysed, from October to April, in the presence and absence of the parasitoid Aphidius rhopalosiphi. In the presence of parasitoids in winter, aphid populations decreased markedly and remained low at the beginning of spring. Induction of winter diapause in A. rhopalosiphi was observed during November at a mean temperature of 6.3°C and a decreasing photoperiod from 9.5–8.5 h of day light. A large range of A. rhopalosiphi mummy colourations, between dark and light, was noticed. This range of colouration did not allow a clear-cut distinction between diapausing and non-diapausing individuals of A. rhopalosiphi. The influence of seasonal weather and particularly temperature conditions on parasitoid mortality, strategy for overwintering and aphid population dynamics are discussed.     

Enhancing biological control by an omnivorous lacewing: Floral resources reduce aphid numbers at low aphid densities

The availability of plant resources to omnivorous arthropod predators may have a positive, negative or negligible effect on their population densities and predation rates, depending on the availability of prey. At high prey densities, flowering buckwheat has been shown to negatively impact populations of the brown lacewing, an omnivorous predator, due to the probable increase in parasitism rate of lacewing larvae by their primary parasitoid, Anacharis zealandica. However, little is known about the effect of buckwheat flowers on this insect community at low prey densities. We used field cages to assess the effects of nectar provision by flowering buckwheat on the population dynamics of the pea aphid, the brown lacewing and its parasitoid A. zealandica in an alfalfa field, under low aphid densities in the New Zealand summer. The insects were sampled every 2 weeks with a suction device, then counted and released on each sampling date from 15 January to 15 March 2007. Buckwheat significantly increased lacewing populations and significantly decreased aphid numbers by 70% and 39%, respectively. The buckwheat had its greatest effect at the end of summer (February/March) for both these species. It had no effect on A. zealandica abundance.     

Nonlinearities Lead to Qualitative Differences in Population Dynamics of Predator-Prey Systems

Since typically there are many predators feeding on most herbivores in natural communities, understanding multiple predator effects is critical for both community and applied ecology. Experiments of multiple predator effects on prey populations are extremely demanding, as the number of treatments and the amount of labour associated with these experiments increases exponentially with the number of species in question. Therefore, researchers tend to vary only presence/absence of the species and use only one (supposedly realistic) combination of their numbers in experiments. However, nonlinearities in density dependence, functional responses, interactions between natural enemies etc. are typical for such systems, and nonlinear models of population dynamics generally predict qualitatively different results, if initial absolute densities of the species studied differ, even if their relative densities are maintained. Therefore, testing combinations of natural enemies without varying their densities may not be sufficient. Here we test this prediction experimentally. We show that the population dynamics of a system consisting of 2 natural enemies (aphid predator Adalia bipunctata (L.), and aphid parasitoid, Aphidius colemani Viereck) and their shared prey (peach aphid, Myzus persicae Sulzer) are strongly affected by the absolute initial densities of the species in question. Even if their relative densities are kept constant, the natural enemy species or combination thereof that most effectively suppresses the prey may depend on the absolute initial densities used in the experiment. Future empirical studies of multiple predator – one prey interactions should therefore use a two-dimensional array of initial densities of the studied species. Varying only combinations of natural enemies without varying their densities is not sufficient and can lead to misleading results.     

Metapopulation dynamics in an aphid-parasitoid system

Metapopulation theory makes a number of predictions concerning the effects of dispersal on the persistence of predator-prey or host-parasitoid systems. While the stabilising effects of dispersal have been shown in a number of laboratory studies, evidence from field studies remains scarce due to a lack of suitable model systems. I describe a host-parasitoid system that shows a classical metapopulation structure with frequent extinctions and colonisations consisting of the aphidiid Lysiphlebus hirticornisand the aphid Metopeurum fuscoviride. Both the parasitoid and the aphid are specialists on their respective hosts. I followed the dynamics of host and parasitoid on individually marked tansy (Tanacetum vulgare) plants, the host of M. fuscoviride. Dynamics of host and parasitoid populations were characterized by frequent extinctions and colonisations. Mean longevity of aphid colonies was only 3.1 weeks. Parasitism by L. hirticorniswas a main cause of extinction for the aphid as rates of parasitism often reached 100%, in particular towards the end of the field season. Patchiness in this system occurs at two spatial scales. Aphid colonies form on single tansy ramets = shoots but movements of aphid individuals among ramets within a particular tansy genet are frequent. Because aphids can persist on a genet for a large numer of generations, it is argued that local populations form on genets rather than ramets. The number of host and parasitoid extinctions described in this study exceeds the number of extinctions usually observed in field studies of host-parasitoid metapopulations. It is suggested that aphid-parasitoid systems such as the one studied in this paper may be good models to test the predictions of metapopulation theory.     

Aphid parasitoid responses to semiochemicals — Genetic, conditioned or learnt?

Parasitoid foraging behaviour is known to be influenced by interactions of genetic, physiological, environmental and experiential factors. Although the role of genetics, learning and conditioning in determining responses to foraging cues has been studied in lepidopteran parasitoids, aphid parasitoids have been less intensively researched. Using the tritrophic system,Vicia faba — Acyrthosiphon pisum — Aphidius ervi, evidence for the role of genetics and learning in parasitoid foraging is presented, and the difficulty of differentiating between genetic responses and those conditioned during parasitoid development is discussed. Aphidius ervi responds to aphid sex pheromones both in the field and in the laboratory. Since laboratory reared individuals have never experienced sexual aphids, the response must be genetic as it cannot have been conditioned during development. An example of a response conditioned during development is the variable response ofA. rhopalosiphi to different wheat cultivars depending upon host feeding. Aphid parasitoids also are adept at learning as shown by their responses to plant-derived cues which are learnt as Conditioned Stimuli (CS). Host products such as honeydew, as well as the host itself, can act as the Unconditioned Stimulus (US) in the learning process. Aphidius ervi offers a good model for investigating the role of these factors in parasitoid foraging behaviour. Finally, the value of such research for biological control programmes involving aphid parasitoids is discussed.     

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e., from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid–symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid–symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host–parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect–symbiont associations.     

Identification of Top-Down Forces Regulating Cotton Aphid Population Growth in Transgenic Bt Cotton in Central China

The cotton aphid Aphis gossypii Glover is the main aphid pest in cotton fields in the Yangtze River Valley Cotton-planting Zone (YRZ) in central China. Various natural enemies may attack the cotton aphid in Bt cotton fields but no studies have identified potential specific top-down forces that could help manage this pest in the YRZ in China. In order to identify possibilities for managing the cotton aphid, we monitored cotton aphid population dynamics and identified the effect of natural enemies on cotton aphid population growth using various exclusion cages in transgenic Cry1Ac (Bt)+CpTI (Cowpea trypsin inhibitor) cotton field in 2011. The aphid population growth in the open field (control) was significantly lower than those protected or restricted from exposure to natural enemies in the various exclusion cage types tested. The ladybird predator Propylaea japonica Thunberg represented 65% of Coccinellidae predators, and other predators consisted mainly of syrphids (2.1%) and spiders (1.5%). The aphid parasitoids Aphidiines represented 76.7% of the total count of the natural enemy guild (mainly Lysiphlebia japonica Ashmead and Binodoxys indicus Subba Rao & Sharma). Our results showed that P. japonica can effectively delay the establishment and subsequent population growth of aphids during the cotton growing season. Aphidiines could also reduce aphid density although their impact may be shadowed by the presence of coccinellids in the open field (likely both owing to resource competition and intraguild predation). The implications of these results are discussed in a framework of the compatibility of transgenic crops and top-down forces exerted by natural enemy guild.     

Aphid Honeydew Quality as a Food Source for Parasitoids Is Maintained in Bt Cotton

Bt-transgenic cotton has proven to be highly efficient in controlling key lepidopteran pests. One concern with the deployment of Bt cotton varieties is the potential proliferation of non-target pests. We previously showed that Bt cotton contained lower concentrations of insecticidal terpenoids as a result of reduced caterpillar damage, which benefited the aphid Aphis gossypii. It is thus important that non-target herbivores are under biological control in Bt cotton fields. The induction or lack of induction of terpenoids could also influence the quality of aphid honeydew, an important food source for beneficial insects. We therefore screened A. gossypii honeydew for cotton terpenoids, that are induced by caterpillars but not the aphids. We then tested the influence of induced insect-resistance of cotton on honeydew nutritional quality for the aphid parasitoid Lysiphlebus testaceipes and the whitefly parasitoid Eretmocerus eremicus. We detected the cotton terpenoids gossypol and hemigossypolone in A. gossypii honeydew. Although a feeding assay demonstrated that gossypol reduced the longevity of both parasitoid species in a non-linear, dose-dependent manner, the honeydew was capable of sustaining parasitoid longevity and reproduction. The level of caterpillar damage to Bt and non-Bt cotton had no impact on the quality of honeydew for the parasitoids.These results indicate that the nutritional quality of honeydew is maintained in Bt cotton and is not influenced by induced insect resistance.     

Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis

Coincidental intraguild predation is expected to be less disruptive to biological control than omnivorous intraguild predation, and strong intraguild predation is not expected to occur in natural systems. Coincidental intraguild predation in a foodweb involving introduced pest and natural enemy species was examined to determine whether intraguild predation would be disruptive of biological control services in soybean agroecosystems. Introduced natural enemies are important regulators of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations in North America. Seven-spotted lady beetles, Coccinella septempunctata L., and multicolored Asian lady beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), are key predators of soybean aphid in North America while the chalcidoid wasp, Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae), is the most common parasitoid of soybean aphid in Ontario, Canada. Predation of parasitized soybean aphids at two stages (newly parasitized aphids and mummified aphids) by adults and third instar larvae of both C. septempunctata and H. axyridis was examined in laboratory experiments. In choice experiments, all stages of lady beetles preferred non-parasitized aphids over mummified aphids. In cage experiments, third instar larvae and male and female adults of both lady beetles did not discriminate between newly parasitized and non-parasitized aphids. The influence of coincidental intraguild predation on the efficacy of parasitoids as biological control agents, and implications for soybean aphid management decisions based on natural enemies, are discussed.     

An implicit approach to model plant infestation by insect pests

Various spatial approaches were developed to study the effect of spatial heterogeneities on population dynamics. We present in this paper a flux-based model to describe an aphid-parasitoid system in a closed and spatially structured environment, i.e. a greenhouse. Derived from previous work and adapted to host-parasitoid interactions, our model represents the level of plant infestation as a continuous variable corresponding to the number of plants bearing a given density of pests at a given time. The variation of this variable is described by a partial differential equation. It is coupled to an ordinary differential equation and a delay-differential equation that describe the parasitized host population and the parasitoid population, respectively. We have applied our approach to the pest Aphis gossypii and to one of its parasitoids, Lysiphlebus testaceipes, in a melon greenhouse. Numerical simulations showed that, regardless of the number and distribution of hosts in the greenhouse, the aphid population is slightly larger if parasitoids display a type III rather than a type II functional response. However, the population dynamics depend on the initial distribution of hosts and the initial density of parasitoids released, which is interesting for biological control strategies. Sensitivity analysis showed that the delay in the parasitoid equation and the growth rate of the pest population are crucial parameters for predicting the dynamics. We demonstrate here that such a flux-based approach generates relevant predictions with a more synthetic formalism than a common plant-by-plant model. We also explain how this approach can be better adapted to test different management strategies and to manage crops of several greenhouses.     

The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression

Intraguild predation (IGP) occurs when consumers competing for a resource also engage in predatory interactions. A common type of IGP involves aphid predators and parasitoids: since parasitoid offspring develop within aphid hosts, they are particularly vulnerable to predation by aphid predators such as coccinellid beetles. Other intraguild interactions that include non-lethal behavioral effects, such as interference with foraging and avoidance of IGP, may also hamper parasitoid activity and reduce their effectiveness as biological control agents. In this study, we quantified mortality in and behavioral effects on Aphidius colemani Viereck (Hymenoptera: Aphidiidae) by its IG-predator Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and compared the impact of two release ratios of these natural enemies on aphid populations. Parasitoids did not leave the plant onto which they were first introduced, regardless of the presence of predators, even when alternative prey was offered on predator-free plants nearby. In 2-hour experiments, predator larvae interfered with wasp activity, and the level of aphid parasitism was lower in the presence of predators than in their absence. In these experiments, the parasitoids contributed more to aphid mortality than the predators and aphid suppression was higher when a parasitoid acted alone than in combination with a predator larva. These results were confirmed in a 5-day experiment, but only at one parasitoid:predator release ratio (4:3) not another (2:3). The over-all impact on aphid population growth was non-the-less stronger when both enemies acted together than when only one of them was present. Results indicate that for given release ratios and time scale, the negative lethal and non-lethal effects of the predator on parasitoid performance did not fully cancelled the direct impact of the predator on the aphid population.     

Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.