Gábor L. Lövei

The impact of transgenic plants on natural enemies: a critical review of laboratory studies

We reviewed laboratory tests which studied the impact of genetically modified plants on arthropod natural enemies. A total of 18 species of predators and 14 species of parasitoids have been tested, most in only a few experiments. Certain groups (braconid wasps) or species (the green lacewing, Chrysoperla carnea) have attracted much effort, while representatives of others, including whole orders (e.g., Diptera), have never had a species tested. We conclude that laboratory tests are not the ‘worst case’ scenarios intended by the experimental designs, and are not often ecologically realistic: they typically provided ad libitum feeding, no prey choice, single prey type, no combination of stress factors and usually uniform temperatures. None of these are representative of field conditions, yet most could be easily mimicked in more complex laboratory tests. In most cases (94.6%), the studies were unable to indicate the level of power required to detect any impact. Small sample size and large variability are factors that mask all but very large differences in potential effects. For predators, 126 parameters were quantified, most commonly including survival/mortality (37 cases), development time (22), and body mass/size (20). For parasitoids, 128 parameters were quantified, the majority involving lectins or proteinase inhibitors. Most frequent measurements were: fecundity (23 experiments), adult longevity, extent of parasitism (17 each), body size, mortality, and larval development time. An aggregative scoring (summarising all quantified parameters) indicated that the laboratory tests quantified a remarkable number of cases (30% for predators, 39.8% for parasitoids), where the impacts of the genetically modified plant were significantly negative. These involve various parameters, organisms, test methods, and significance levels, but collectively they indicate that the use of genetically modified crops may result in negative effects on the natural enemies of crop pests.

Forty years of carabid beetle research in Europe – from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation

Abstract ‘Carabidologists do it all’ (Niemelä 1996a) is a phrase with which most European carabidologists are familiar. Indeed, during the last half a century, professional and amateur entomologists have contributed enormously to our understanding of the basic biology of carabid beetles. The success of the field is in no small part due to regular European Carabidologists’ Meetings, which started in 1969 in Wijster, the Netherlands, with the 14th meeting again held in the Netherlands in 2009, celebrating the 40th anniversary of the first meeting and 50 years of long-term research in the Dwingelderveld. This paper offers a subjective summary of some of the major developments in carabidology since the 1960s. Taxonomy of the family Carabidae is now reasonably established, and the application of modern taxonomic tools has brought up several surprises like elsewhere in the animal kingdom. Progress has been made on the ultimate and proximate factors of seasonality and timing of reproduction, which only exceptionally show non-seasonality. Triggers can be linked to evolutionary events and plausibly explained by the “taxon cycle” theory. Fairly little is still known about certain feeding preferences, including granivory and ants, as well as unique life history strategies, such as ectoparasitism and predation on higher taxa. The study of carabids has been instrumental in developing metapopulation theory (even if it was termed differently). Dispersal is one of the areas intensively studied, and results show an intricate interaction between walking and flying as the major mechanisms. The ecological study of carabids is still hampered by some unresolved questions about sampling and data evaluation. It is recognised that knowledge is uneven, especially concerning larvae and species in tropical areas. By their abundance and wide distribution, carabid beetles can be useful in population studies, bioindication, conservation biology and landscape ecology. Indeed, 40 years of carabidological research have provided so much data and insights, that among insects - and arguably most other terrestrial organisms - carabid beetles are one of the most worthwhile model groups for biological studies.

Transgenic Insecticidal Crops and Natural Enemies: A Detailed Review of Laboratory Studies

ABSTRACT This review uses a data-driven, quantitative method to summarize the published, peer-reviewed literature about the impact of genetically modified (GM) plants on arthropod natural enemies in laboratory experiments. The method is similar to meta-analysis, and, in contrast to a simple author-vote counting method used by several earlier reviews, gives an objective, data-driven summary of existing knowledge about these effects. Significantly more non-neutral responses were observed than expected at random in 75% of the comparisons of natural enemy groups and response classes. These observations indicate that Cry toxins and proteinase inhibitors often have non-neutral effects on natural enemies. This synthesis identifies a continued bias toward studies on a few predator species, especially the green lacewing, Chrysoperla cornea Stephens, which may be more sensitive to GM insecticidal plants (16.8% of the quantified parameter responses were significantly negative) than predators in general (10.9% significantly negative effects without C. cornea). Parasitoids were more susceptible than predators to the effects of both Cry toxins and proteinase inhibitors, with fewer positive effects (18.0%, significant and nonsignificant positive effects combined) than negative ones (66.1%, significant and nonsignificant negative effects combined). GM plants can have a positive effect on natural enemies (4.8% of responses were significantly positive), although significant negative (21.2%) effects were more common. Although there are data on 48 natural enemy species, the database is still far from adequate to predict the effect of a Bt toxin or proteinase inhibitor on natural enemies.

Global change through invasion

Humans have, for many thousands of years, introduced crops and animals into different parts of the world. But the introduction of many species has not been so welcome, and today more species are being introduced than ever before. A new report warns that these introductions are an important component of human-induced global change, and that they represent a serious threat to biodiversity.

Conservation Focus on Europe: Major Conservation Policy Issues That Need to Be Informed by Conservation Science

Europe is one of the worlds most densely populated continents and has a long history of human-dominated land- and seascapes. Europe is also at the forefront of developing and implementing multinational conservation efforts. In this contribution, we describe some top policy issues in Europe that need to be informed by high-quality conservation science. These include evaluation of the effectiveness of the Natura 2000 network of protected sites, implications of rapid economic and subsequent land-use change in Central and Eastern Europe, conservation of marine biodiversity and sustainability of fisheries, the effect of climate change on movement of species in highly fragmented landscapes, and attempts to assess the economic value of ecosystem services and biodiversity. Broad policy issues such as those identified are not easily amenable to scientific experiment. A key challenge at the science-policy interface is to identify the research questions underlying these problem areas so that conservation science can provide evidence to underpin future policy development.

The influence of matrix and edges on species richness patterns of ground beetles (Coleoptera: Carabidae) in habitat islands

Aim The aim of this study was to analyse whether, and how, the inclusion of habitat specialists and edge-preferring species modifies the species–area relationship predictions of the island biogeography theory for an insect group (ground beetles, Coloptera: Carabidae) living in natural fragments. Species–habitat island area relationships applied to terrestrial habitat islands can be distorted by the indiscriminate inclusion of all species occurring in the fragments. Matrices surrounding terrestrial habitat fragments can provide colonists that do not necessarily distinguish the fragment from the matrix and can survive and reproduce there. Edge-preferring species can further distort the expected relationship, as smaller fragments have larger edge:core ratios. Location Nineteen forest fragments were studied in the Bereg Plain, Hungary, and SW Ukraine. This area contains natural forest patches, mainly of oak and hornbeam, and supports a mountain entomofauna. Methods Ground beetles (Carabidae) present in the 19 forest patches were categorized into generalists, forest specialists and edge-preferring species. We analysed the relationship between species richness and fragment area using species richness in the different categories. Results The assemblages contained a high share of generalist species (species that occur also in the surrounding matrix). Forest patch size and the number of generalist species showed a marginally significant negative relationship, indicating that generalist species were more important in smaller patches. Forest specialist species richness was correlated positively with patch area. Edge-preferring species were shown to influence the species–area relationship: the number of edge-preferring species increased with the edge:area ratio. Main conclusions Both generalist and edge-preferring species can considerably distort the species–area relationship. Island biogeography theory can be applied to habitat islands only if the habitat islands are defined correctly from the viewpoint of the target species.

Ecosystem services and biodiversity in developing countries

The concept of ecosystem services has become important for our understanding of the role of nature for maintaining human livelihoods. But is biodiversity essential to maintain ecosystem services? Many studies suggest that higher biodiversity allows a higher level of ecosystem services, but others argue that there is little hard evidence, especially from tropical environments, to document the necessity of high biodiversity for provision of most ecosystem services. Thus, effective valuation of biodiversity for ecosystem services and long-term studies and monitoring are needed to fully understand the complex biodiversity-ecosystem service interface. This introduction briefly reviews some of the main arguments in this debate and provides an overview of the other five special issue papers. Exploring biodiversity and ecosystem interactions in the context of the provision of ecosystem services, these papers address population and biodiversity coexistence, the importance of dung beetles in agricultural landscapes, the knowledge and use of palms by local communities, bioprospecting for drugs and how biodiversity conservation may have added benefits in terms of improved watershed functions and health.

Transmission of Bt Toxin to the Predator Propylaea japonica (Coleoptera: Coccinellidae) Through Its Aphid Prey Feeding on Transgenic Bt Cotton

Abstract Laboratory feeding experiments using transgenic Bacillus thuringiensis (Bt) cotton plants were carried out to evaluate the transmission of Bt toxin among trophic levels and the effects of Bt-fed herbivorous prey on the coccinellid predator Propylaea japonica (Thunberg). The experimental host plants were transgenic Bt-expressing cotton cultivars, NuCOTN 33B and GK-12 and one corresponding untransformed isogenic (non-Bt) cultivar. The herbivorous prey, cotton aphid Aphis gossypii Glover, was not sensitive to Bt toxin. Trace amounts of Bt toxins (6.0 ng/g fresh mass [FM] in GK-12, 4.0 ng/g FM in NuCOTN 33B) were detected in A. gossypii feeding on Bt cotton cultivars. Bt toxin was detected in ladybirds preying on Bt-fed aphids, and its quantity increased as the predatory period extended (5–20 d). Small amounts of Bt toxin was also found in newly hatched, unfed coccinellid larvae when their parents fed on NuCOTN 33B-reared aphids (15.0 ng/g FM), but not when the parents were fed on GK-12–reared prey. In experiments assessing life history consequences, mortality was low (mean = 7.9%), confirming that the rearing methods were appropriate. There were no distinct differences in preimaginal mortality between predators reared on Bt-fed or Bt-free aphids. The preimaginal stages of the ladybird beetles developed faster when reared on prey fed on either Bt-cotton cultivar than those fed control prey. There was a trend of more adult malformations when the predator was fed with prey from one (GK-12) but not the other of the Bt cotton cultivars than on control prey. There were no significant differences in the preovipositing period or in fecundity. Ladybird beetles preying on Bt-reared aphids matured faster and mated more frequently than those fed on Bt-free aphids. These results indicate that Bt toxin expressed in transgenic cotton cultivars can be transmitted to a higher trophic level through a nontarget pest insect and may alter the biology and behavior of a predatory ladybird. Further work should evaluate the possible long-term, sublethal impacts on the agroenvironment under field conditions.

Dummy caterpillars as a simple method to assess predation rates on invertebrates in a tropical agroecosystem

Attention to the role ecosystem services play in main-taining the world’s habitats and their inhabitants isincreasing as both our understanding and opportunitiesto estimate the economic value of these services increase.Generally, these services are of immense importance,not only from an anthropogenic viewpoint; they are alsonecessary to maintain the health and functioning of eco-systems (MA, 2005). The recently completed Millen-nium Ecosystem Assessment highlighted the need formethods to evaluate these services, but existing knowl-edge already indicates that many ecosystem services arenot in good shape (MA, 2005).Agricultural management is very important from thisperspective (Tilman et al., 2002; Dale & Polasky, 2007).Ecosystem services tend to be more important in devel-oping than in developed countries (Mertz et al., 2007),mainly (but not only) because in those agroecosystems,external resources are often not available to substitutefor ecosystem services, especially in rural communities(Mertz et al., 2007). Biological control⁄natural pest con-trol through predation and parasitism by an array ofnaturally occurring organisms (native natural enemies)is one of the recognised ecosystem services (de Grootet al., 2002). However, our knowledge about the level ofbiological control provided by ecosystems is not toodetailed, and especially lacking from developing coun-tries in the tropics.Studies on natural enemies often assume density as ameasure of natural enemy importance or intensity offunction (Waage & Mills, 1992), arguing that a doublingin natural enemy densities equates to a two-fold increasein predation pressure. This is not necessarily so, becauseseveral factors, including predator satiation, intraguildpredation, and intra- and interspecific competition cancomplicate the picture (Schmitz, 2007). Therefore, thereis a need for functional biological control studies whichmeasure levels of natural enemy pressure on pests underfield conditions. Natural enemy activity in general is dif-ficult to detect, especially by invertebrates. Assessingparasitism rates is less problematic because the hosts ofparasitoids often become immobile and are easily recog-nised. However, predation often leaves no trace, or onlyfragments of the consumed prey can be found. A preda-tion event usually happens quickly, predators often hidewhile consuming prey, and many of them are active atnight (Crawley, 1992). Such factors make field assess-ments of predation intensity difficult. These inherentproblems have curtailed our knowledge about the kindand extent of predation in different habitats by differentnatural enemies (Crawley, 1992). Consequently, we haveseveral examples of quantitative parasitoid food webs(Mu¨ller et al., 1999), but fewer of predator food webs.Predation can be studied by video recording (Varleyet al., 1994), by indirect means, using dyes, markers,and analysis of predators for prey remains, or by usingsentinel prey (Jervis & Kidd, 1996). The last methodmonitors the rate of disappearance of prey provided bythe experimenter, and is the easiest one to obtain quan-titative data on predation pressure. Immobile (eggs,pupae) or immobilised stages of arthropods are oftenused as sentinel prey. This approach has several inherentproblems, such as generating sufficient numbers (whichoften requires mass rearing), putting them out into thefield, and recording⁄identifying the natural enemiesresponsible for prey disappearance. Several of the abovedifficulties can be avoided or circumvented if artificial

Digestion rate in relation to starvation in the larva of a carabid predator, Poecilus cupreus

Prey antigen levels were determined by a quantitative enzyme‐linked immunosorbent assay in larvae of a carabid predator, Poecilus cupreus L. under laboratory conditions. We determined prey consumption and rate of prey protein decay in larvae having starved for different periods. Prey consumption increased exponentially over 7 days of starvation. The rate of prey immunoreactive material decay seemed to be logarithmic, similar in larvae which had starved for different periods. Most of the digestion took place in the first 3 days period after feeding, irrespective of the amounts ingested. The rate of decay increased with increasing period of starvation. There were also signs of food retention in the alimentary canal in larvae which starved longer.