Dirk Babendreier

Benefits and risks of exotic biological control agents

The use of exotic (=alien) arthropods in classical and augmentative biological control programs has yielded huge economic and ecological benefits. Exotic species of arthropods have contributed to the suppression of key pests in agriculture and forestry or have aided in restoring natural systems affected by adventive species. However, adverse non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, e.g. 2% parasitization on a non-target insect on a local level, to massive effects on a large scale. Until now, no consensus on how to judge the magnitude of non-target effects and whether these effects can be tolerated or are unacceptable has emerged. In this paper, we briefly review both the benefits of biological control as well as the associated risks including to human and animal health, plant health and particularly the environment. We also make an attempt at identifying the major challenges for assessing risks and for balancing benefits and risks. There is general agreement that sound risk assessment procedures should precede the release of exotic invertebrate biological control agents and a recent shift—especially for arthropod biological control—from introductions done without meaningful risk assessment studies to projects conducting thorough host range testing can be observed. However, overly stringent regulations that would preclude promising agents from being developed must be avoided.

Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species

The coccinellid Harmonia axyridis (Pallas) has been used for augmentative and classical biological control in many environments. More recently it has invaded large parts of Europe and negative effects for native populations of aphidophagous coccinellids are beginning to emerge. Here we investigate intraguild predation (IGP) between H. axyridis and eleven native non-target European coccinellids, including less common species which have not been studied so far within this context of non-target effects. When first-instars of H. axyridis were paired with the native species, only Anatis ocellata (Linnaeus) and Calvia quatuordecimguttata (L.) were significantly superior to the former whereas H. axyridis was superior in three cases, i.e. against Aphidecta obliterata (L.), Coccinella septempunctata L. and Hippodamia variegata (Goeze). Non-significant results were obtained for all other pairings. Similar tests with the fourth larval instar revealed stronger IGP rates and H. axyridis was found to be superior in the interactions with Adalia bipunctata (L.), Adalia decempunctata (L.), A. obliterata, Calvia decemguttata (L.), C. quatuordecimguttata, C. septempunctata, H. variegata, Oenopia conglobata (L.) and Propylea quatuordecimpunctata (L.) whereas non-significant results were obtained for interactions with two other native species. Another experiment revealed that H. axyridis was able to prey more successfully upon egg of most native coccinellid species than vice versa. However, C. quatuordecimguttata eggs seem to be more protected against predation than those of the other species. Survival of first-instar H. axyridis was higher on conspecific eggs compared to eggs of any other species tested. Our results suggest that H. axyridis may become a threat to a wide range of native aphidophagous coccinellids sharing similar ecological niches except species showing high potential for chemical or physical protection.

Effects of multiple Bt proteins and GNA lectin on in vitro-reared honey bee larvae

The honey bee is a key non-target arthropod in environmental risk assessments of genetically modified crops. We analyzed for the first time combined effects of three Bt proteins conferring insect resistances, and a CP4-protein conferring an herbicide resistance as simultaneously expressed in one GM maize. Furthermore, the biosafety of Galanthus nivalis agglutinin (GNA lectin), a candidate protein for pest control was tested. Under worst-case exposure scenario, by using controlled in vitro larvae rearing, the combination of Bt proteins showed no adverse effects on bee larvae. In contrast, the GNA lectin was toxic at a 144xa0h LD50 of 16.3xa0μg/larva. The prepupal weight was found to differ between the larvae collection days and between the colonies used for the experiment, explaining up to five times more data variance than the protein treatments (Nu2009=u2009709 prepupae). In conclusion, neither single nor a mix of different Bt proteins were found harmful to honey bee larvae.

Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study

Invasive alien predators are a serious threat to biodiversity worldwide. However, there is no generic method for assessing which local species are most at risk following the invasion of a new predator. The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is an alien in Europe and many other parts of the world where it affects other species of ladybirds through competition for food and intra-guild predation (IGP). Here, we describe a method developed to assess which European ladybird species are most at risk following the invasion of H. axyridis. The three components of the risk assessment are: the likelihood that the assessed native species encounters H. axyridis in the field, the hazard of competition for food, and the IGP hazard. Thirty native European ladybird species were assessed through data obtained from field observations, laboratory experiments and literature reviews. The species that are considered most at risk are found on deciduous trees, have immature stages which are highly vulnerable to IGP by H. axyridis, and are primarily aphidophagous. These species should be the focus of specific studies and possibly conservation actions. The risk assessment method proposed here could be applied to other alien predators which are considered a threat to native species through competition and predation.

Evaluation for Potential Trichogramma (Hymenoptera: Trichogrammatidae) Strains for Control of the Striped Stem Borer (Lepidoptera: Crambidae) in the Greater Mekong Subregion

ABSTRACT Trichogramma species and strains differ significantly in host specificity and performance. Nine Trichogramma strains, six of them collected from paddy fields in the Greater Mekong Subregion, were evaluated for performance on eggs of the striped stem borer, Chilo suppressalis (Walker), in both laboratory and field tests to determine potential Trichogramma strains that can be used in an inundative release in an integrated pest management program. In the laboratory glass vial tests, all strains showed higher parasitism rates on 0 -24-h eggs than on the two older age groups (24–48 and 48–72 h). Wasp emergence rate was also higher from parasitized 0-24-h striped stem borer eggs, while Trichogramma immature duration was significantly prolonged on 0-24-h striped stem borer eggs. Parasitism rates differed among Trichogramma strains, with Trichogramma chilonis Ishii CJ strain showing significantly higher parasitism rate than any other strains. In the field tests, parasitism of sentinel striped stem borer eggs by Trichogramma strains released at 50,000,100,000, and 200,000 wasps per hectare was low, with marginal yet significant differences between strains. The highest parasitism was achieved by T. chilonis CJ strain at the high and medium release rates. Hence, it can be concluded that T. chilonis CJ strain released at 100,000 wasps per hectare may be a cost-effective control tactic for field releases targeting striped stem borer.

Toxicity of Insecticides Targeting Rice Planthoppers to Adult and Immature Stages of Trichogramma chilonis (Hymenoptera: Trichogrammatidae).

ABSTRACT Planthopper-targeting insecticides, pymetrozine, thiamethoxam, buprofezin, and nitenpyram, were tested under laboratory conditions for toxicity to adults and immatures of Trichogramma chilonis Ishii, using standard tests described by International Organization for Biological Control (IOBC). In the dry film residue test, all insecticides resulted in >90% mortality in T. chilonis adults and were ranked as moderately harmful. Persistent toxicity tests revealed that nitenpyram was short-lived and the other three insecticides were of slightly persistent toxicity to the wasp adults. Effects of the insecticides on egg, larval, and prepupal stages of T. chilonis were investigated with striped stem borer as host. At the three stages of T. chilonis (within the host egg), all the insecticides reduced parasitism rate, but nitenpyram and pymetrozine applied at egg stage, buprofezin and nitenpyram at larval stage, and buprofezin and thiamethoxam at prepupal stage of T. chilonis reduced parasitism by <30% in comparison with the control, and were thus ranked as harmless. Although insecticide treatment of the three immature stages of T. chilonis all reduced wasp emergence from host eggs, only thiamethoxam applied at larval stage and buprofezin at prepupal stage resulted in >30% reduction in emergence rate as compared with the control and were categorized as harmful. Immature duration of T. chilonis was only significantly extended by nitenpyram applied to egg stage than the control. Sex ratio of emerged wasps was not affected by the treatment to immature stages. The data are of significance for IPM programs incorporating inundative release of T. chilonis for control of lepidopteran rice pests where there is heavy co-occurrence of planthoppers.

Chemical defences of native European coccinellid eggs against intraguild predation by the invasive Asian coccinellid, Harmonia axyridis (Pallas)

Harmonia axyridis (Pallas) is a coccinellid of Asian origin that has recently invaded substantial parts of Europe and is suspected to affect native coccinellid populations through intraguild predation and competition for food. Previous work has shown that two species from the Calvia genus appeared to be well protected against H.xa0axyridis predation. To deepen our understanding on chemical protection of Calvia spp. and the predation risk by H.xa0axyridis, we tested for susceptibility and palatability of Calvia spp. and H.xa0axyridis eggs against predation by H.xa0axyridis neonate larvae. Results show that eggs of C.xa0quatuordecimguttata were mostly not eaten by H.xa0axyridis, while eggs of the congeneric C.xa0decemguttata were found to be largely unprotected against predation by the invasive coccinellid. We also observed that H.xa0axyridis first instars successfully cannibalized on conspecific eggs. Removing the surface chemicals from C.xa0quatuordecimguttata eggs resulted in significantly reduced protection from being preyed upon by H.xa0axyridis, while applying these extracts onto C.xa0decemguttata and H.xa0axyridis eggs resulted in increased protection against H.xa0axyridis larvae. The importance of surface chemicals in the interactions between H.xa0axyridis and native coccinellids was confirmed by GC–MS analysis, showing a high diversity of hydrocarbons located on the surface of C.xa0quatuordecimguttata eggs, i.e. more than twice as many when compared to C.xa0decemguttata. Survival of H.xa0axyridis larvae feeding on eggs of C.xa0quatuordecimguttata, C.xa0decemguttata or conspecific eggs, from which surface chemicals were removed by washing them with hexane, was not different from survival on unwashed eggs.

Assessment of Trichogramma japonicum and T. chilonis as Potential Biological Control Agents of Yellow Stem Borer in Rice

Two species of Trichogramma wasps were assessed for their effectiveness against yellow stem borer Scirpophaga incertulas. A laboratory cage test with T. japonicum and T. chilonis showed that both species parasitized yellow stem borer egg masses at 60.0% ± 9.13% and 40.7% ± 7.11%, respectively, with egg parasitism rates of 15.8% ± 22.2% for T. japonicum and 2.8% ± 5.0% for T. chilonis. Once the host eggs were parasitized, emergence rates were high for both species (95.7% ± 0.12% for T. japonicum and 100% for T. chilonis). In paddy field trials, the two Trichogramma species were released at three densities (50,000/ha, 100,000/ha and 200,000/ha) in Southwestern China. Egg mass parasitism was 9% ± 7.7% for T. japonicum and 15% ± 14.1% for T. chilonis, and again only a relatively small fraction of eggs was successfully parasitized. No clear conclusion could be drawn on the most efficient release rate as no significant differences were found among the three release rates. A comparison of field-collected T. japonicum with T. japonicum and T. chilonis mass reared on Corcyra cephalonica showed significantly larger body size and ovipositor length in field-collected wasps, suggesting potentially higher effectiveness on yellow stem borer eggs after at least one generation on the target host. Factors contributing to the low field parasitism rates are discussed.

Using the egg parasitoid Anastatus bifasciatus against the invasive brown marmorated stink bug in Europe: can non-target effects be ruled out?

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has been causing massive damage to various fruit and vegetable crops after its arrival in the USA, and more recently in Europe. To provide an alternative control measure to pesticides, the native egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) was considered as a candidate biological control agent for inundative releases in Europe. In the risk assessment study presented here, all nine heteropteran and 14 out of 19 tested lepidopteran non-target species produced viable A. bifasciatus offspring. The proportion of A. bifasciatus females producing offspring did not differ between non-target and target for 19 out of the 28 non-target species. Larger host eggs corresponded to increased female-biased sex ratio of the offspring as well as an increase in size, particularly for females, with hind tibia lengths varying from 645.5u2009±u200946 to 1084u2009±u200928.5xa0μm. Larger females were also found to have higher offspring production and increased life expectancy. The results of this study confirmed the polyphagous nature of A. bifasciatus and suggest that a number of non-target species, including Lepidoptera of conservation interest, may be attacked in the field. Thus, non-target effects cannot entirely be ruled out, but more information is needed from semi-field and field studies to fully assess potential environmental risks due to inundative releases of this native parasitoid.

Development and fecundity of Trissolcus japonicus on fertilized and unfertilized eggs of the brown marmorated stink bug, Halyomorpha halys

Halyomorpha halys, the brown marmorated stink bug, is a serious agricultural and horticultural pest native to East Asia, which became an invasive pest in northern temperate parts of other regions in the mid-1990s. Trissolcus japonicus is a dominant egg parasitoid of H. halys in its native range. In this paper, we investigated mating, oviposition and fecundity of both virgin and mated females of H. halys. Virgin H. halys females produced unfertilized eggs, while mated females produced fertilized eggs, but mating states of adult females did not affect the number of eggs produced. We further compared the development and fecundity of T. japonicus on fertilized or unfertilized eggs of various ages. Fertilized eggs were tested continuously for up to 5xa0days (time to hatch), while unfertilized eggs were tested for up to 11xa0days (time to egg collapse). The fertilization status of the host egg had a significant effect on the development, emergence success, and sex ratio of T. japonicus progeny. A small increase in development time was observed for T. japonicus in fertilized eggs, fewer T. japonicus emerged from fertilized eggs than unfertilized eggs, and the proportion of female progeny was lower on fertilized eggs. The age of host eggs also significantly affected the development rate and fecundity of T. japonicus, with unfertilized eggs becoming more favorable than fertilized eggs as egg age increased. In summary, unfertilized H. halys eggs were better suited for T. japonicus development and fecundity, indicating their potential use in T. japonicus mass rearing.