Do releases of the mirid predator Macrolophus basicornis (Hemiptera: Miridae) together with the egg parasitoid Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) improve biological control of Tuta absoluta (Lepidoptera: Gelechiidae) in tomato?

During the past decade, the use of predatory mirids alone or combined with releases of egg parasitoids of the genus Trichogramma have been tested in Europe for biological control of the worldwide invasive pest, Tuta absoluta (Meyrick). Here, we evaluated the control of this pest by the release of the Neotropical mirid Macrolophus basicornis (Stal), the Neotropic/Nearctic parasitoid Trichogramma pretiosum Riley, and by combined releases of the predator and the parasitoid. Tests were conducted in greenhouse compartments during the summer and fall season. Each compartment contained 10 tomato plants in which only the pest was released or the pest with 1 or 2 natural enemies. Plant damage, and pest and natural enemy densities were checked weekly on one apical, medium, and bottom leaf of 5 plants. Both M. basicornis and T. pretiosum significantly reduced T. absoluta density when released alone. Combined releases resulted in a 10% higher reduction during the summer season, but not during the fall season. The damage caused by T. absoluta was significantly higher in control treatments than in all natural enemy treatments: at the end of the summer trial leaves were completely damaged in the control treatment, whereas only up to 25% leaf damage occurred in the natural enemy treatments. Combined releases did not result in lower damage than with releases of either M. basicornis or T. pretiosum. Practical aspects of single and combined releases are discussed.

The pest kill rate of thirteen natural enemies as aggregate evaluation criterion of their biological control potential of Tuta absoluta.

Ecologists study how populations are regulated, while scientists studying biological pest control apply population regulation processes to reduce numbers of harmful organisms: an organism (a natural enemy) is used to reduce the population density of another organism (a pest). Finding an effective biological control agent among the tens to hundreds of natural enemies of a pest is a daunting task. Evaluation criteria help in a first selection to remove clearly ineffective or risky species from the list of candidates. Next, we propose to use an aggregate evaluation criterion, the pest kill rate, to compare the pest population reduction capacity of species not eliminated during the first selection. The pest kill rate is the average daily lifetime killing of the pest by the natural enemy under consideration. Pest kill rates of six species of predators and seven species of parasitoids of Tuta absoluta were calculated and compared. Several natural enemies had pest kill rates that were too low to be able to theoretically reduce the pest population below crop damaging densities. Other species showed a high pest reduction capacity and their potential for practical application can now be tested under commercial crop production conditions.

Comparative Effectiveness and Injury to Tomato Plants of Three Neotropical Mirid Predators of Tuta absoluta (Lepidoptera: Gelechiidae).

Tuta absoluta (Meyrick; Lepidoptera: Gelechiidae) is a key pest of tomato and is quickly spreading over the world. We conducted an experiment aimed at evaluating the control capacity and risk for plant damage of three Neotropical mirid species, Campyloneuropsis infumatus (Carvalho; Hemiptera: Miridae), Engytatus varians (Distant; Hemiptera: Miridae) and Macrolophus basicornis (Stal; Hemiptera: Miridae) on T. absoluta infested tomato plants in large cages in an experimental greenhouse. During three successive periods of 9 wk each, we followed population development of the three mirids when exposed to T. absoluta, and of T. absoluta alone in separate cages in the greenhouse. We determined weekly the numbers of T. absoluta eggs and larvae per leaf, the number of mirid predators per leaf, the percentage of damaged leaves and fruits by T. absoluta, and the weight of fruits. Two of the mirid predators, C. infumatus and M. basicornis, successfully established on T. absoluta infested tomato plants and significantly reduced T. absoluta numbers, which ultimately resulted in an increased yield. These two mirid species hardly injured tomato plants or fruits as a result of plant feeding. Surprisingly, the species E. varians, which showed high predation rates in laboratory experiments, did not establish and reduce pest populations in any of the tests.

Attraction of Three Mirid Predators to Tomato Infested by Both the Tomato Leaf Mining Moth Tuta absoluta and the Whitefly Bemisia tabaci.

Plants emit volatile compounds in response to insect herbivory, which may play multiple roles as defensive compounds and mediators of interactions with other plants, microorganisms and animals. Herbivore-induced plant volatiles (HIPVs) may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. We report here the first evidence of the attraction of three Neotropical mirid predators (Macrolophus basicornis, Engytatus varians and Campyloneuropsis infumatus) toward plants emitting volatiles induced upon feeding by two tomato pests, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci, in olfactometer bioassays. Subsequently, we compared the composition of volatile blends emitted by insect-infested tomato plants by collecting headspace samples and analyzing them with GC-FID and GC-MS. Egg deposition by T. absoluta did not make tomato plants more attractive to the mirid predators than uninfested tomato plants. Macrolophus basicornis is attracted to tomato plants infested with either T. absoluta larvae or by a mixture of B. tabaci eggs, nymphs and adults. Engytatus varians and C. infumatus responded to volatile blends released by tomato plants infested with T. absoluta larvae over uninfested plants. Also, multiple herbivory by T. absoluta and B. tabaci did not increase the attraction of the mirids compared to infestation with T. absoluta alone. Terpenoids represented the most important class of compounds in the volatile blends and there were significant differences between the volatile blends emitted by tomato plants in response to attack by T. absoluta, B. tabaci, or by both insects. We, therefore, conclude that all three mirids use tomato plant volatiles to find T. absoluta larvae. Multiple herbivory did neither increase, nor decrease attraction of C. infumatus, E. varians and M. basicornis. By breeding for higher rates of emission of selected terpenes, increased attractiveness of tomato plants to natural enemies may improve the effectiveness of biological control.

Response of a Predatory ant to Volatiles Emitted by Aphid- and Caterpillar-Infested Cucumber and Potato Plants.

In response to herbivory by insects, various plants produce volatiles that attract enemies of the herbivores. Although ants are important components of natural and agro-ecosystems, the importance of herbivore-induced plant volatiles (HIPVs) as cues for ants for finding food sources have received little attention. We investigated responses of the ant Formica pratensis to volatiles emitted by uninfested and insect-infested cucumber (Cucumis sativus) and potato (Solanum tuberosum) plants. Cucumber plants were infested by the phloem-feeding aphid Aphis gossypii, the leaf chewer Mamestra brassicae or simultaneously by both insects. Potato plants were infested by either Aphis gossypii, by the leaf chewer Chrysodeixis chalcites or both. In olfactometer experiments, ants preferred volatile blends emitted by cucumber plants infested with M. brassicae caterpillars alone or combined with A. gossypii to volatiles of undamaged plants or plants damaged by A. gossypii only. No preference was recorded in choice tests between volatiles released by aphid-infested plants over undamaged plants. Volatiles emitted by potato plants infested by either C. chalcites or A. gossypii were preferred by ants over volatiles released by undamaged plants. Ants did not discriminate between potato plants infested with aphids and caterpillars over plants infested with aphids only. Plant headspace composition showed qualitative and/or quantitative differences between herbivore treatments. Multivariate analysis revealed clear separation between uninfested and infested plants and among herbivore treatments. The importance of HIPVs in indirect plant defence by ants is discussed in the context of the ecology of ant-plant interactions and possible roles of ants in pest management.

Functional Responses of Three Neotropical Mirid Predators to Eggs of Tuta absoluta on Tomato.

Tuta absoluta (Meyrick) has quickly developed into a significant tomato pest worldwide. While the recently found mirid predators Macrolophus basicornis (Stal), Engytatus varians (Distant) and Campyloneuropsis infumatus (Carvalho) of this pest are able to establish and reproduce on tomato, biological knowledge of these mirids is still limited. Here we describe the functional response of the three mirid predators of the tomato pest T. absoluta when offered a range of prey densities (four, eight, 16, 32, 64, 128 and 256 eggs) during a 24 h period inside cylindrical plastic cages in the laboratory. Engytatus varians and M. basicornis showed a type III functional response, whereas C. infumatus showed a type II functional response. At the highest prey densities, C. infumatus consumed an average of 51.0 eggs, E. varians 91.1 eggs, and M. basicornis 100.8 eggs. Taking all information into account that we have collected of these three Neotropical mirid species, we predict that M. basicornis might be the best candidate for control of the tomato borer in Brazil: it has the highest fecundity, the largest maximum predation capacity, and it reacts in a density-dependent way to the widest prey range.

Insects Can Count: Sensory Basis of Host Discrimination in Parasitoid Wasps Revealed.

The solitary parasitoid Leptopilina heterotoma is one of the best studied organisms concerning the ecology, behaviour and physiology of host discrimination. Behavioural evidence shows that L. heterotoma uses its ovipositor to discriminate not only between parasitized and unparasitized Drosophila melanogaster larvae, but also to discriminate between hosts with different numbers of parasitoid eggs. The existing knowledge about how and when the parasitoid marks the host motivated us to unravel the chemosensory basis of host discrimination by L. heterotoma that allows it to choose the "best" host available. In this paper we report on electrophysiological recordings of multi-neural responses from the single taste sensillum on the tip of the unpaired ovipositor valve. We stimulated this sensillum with haemolymph of unparasitized, one-time-parasitized and two-times-parasitized Drosophila larvae. We demonstrate for the first time that quantitative characteristics of the neural responses to these haemolymph samples differed significantly, implying that host discrimination is encoded by taste receptor neurons in the multi-neuron coeloconic ovipositor sensillum. The activity of three of the six neurons present in the sensillum suffices for host discrimination and support the hypothesis that L. heterotoma females employ an ensemble code of parasitization status of the host.

The Influence of Vegetation and Landscape Structural Connectivity on Butterflies (Lepidoptera: Papilionoidea and Hesperiidae), Carabids (Coleoptera: Carabidae), Syrphids (Diptera: Syrphidae), and Sawflies (Hymenoptera: Symphyta) in Northern Italy Farmland.

Landscape structure as well as local vegetation influence biodiversity in agroecosystems. A study was performed to evaluate the effect of floristic diversity, vegetation patterns, and landscape structural connectivity on butterflies (Lepidoptera: Papilionoidea and Hesperiidae), carabids (Coleoptera: Carabidae), syrphids (Diptera: Syrphidae), and sawflies (Hymenoptera: Symphyta). Vegetation analysis and insect samplings were carried out in nine sites within an intensively farmed landscape in northern Italy. Plant species richness and the percentage of tree, shrub, and herb cover were determined by means of the phytosociological method of Braun-Blanquet. Landscape structural connectivity was measured as the total length of hedgerow network (LHN) in a radius of 500 m around the center of each sampling transect. Butterflies species richness and abundance were positively associated both to herb cover and to plant species richness, but responded negatively to tree and shrub cover. Shrub cover was strictly correlated to both species richness and activity density of carabids. The species richness of syrphids was positively influenced by herb cover and plant richness, whereas their abundance was dependent on ligneous vegetation and LHN. Rarefaction analysis revealed that sawfly sampling was not robust and no relationship could be drawn with either vegetation parameters or structural connectivity. The specific responses of each insect group to the environmental factors should be considered in order to refine and optimize landscape management interventions targeting specific conservation endpoints.

Movement behaviour of the carabid beetle Pterostichus melanarius in crops and at a habitat interface explains patterns of population redistribution in the field.

Animals may respond to habitat quality and habitat edges and these responses may affect their distribution between habitats. We studied the movement behaviour of a ground-dwelling generalist predator, the carabid beetle Pterostichus melanarius (Illiger). We performed a mark-recapture experiment in two adjacent habitats; a large plot with oilseed radish (Raphanus sativus) and a plot with rye (Secale cereale). We used model selection to identify a minimal model representing the mark-recapture data, and determine whether habitat-specific motility and boundary behaviour affected population redistribution. We determined movement characteristics of P. melanarius in laboratory arenas with the same plant species using video recording. Both the field and arena results showed preference behaviour of P. melanarius at the habitat interface. In the field, significantly more beetles moved from rye to oilseed radish than from radish to rye. In the arena, habitat entry was more frequent into oilseed radish than into rye. In the field, movement was best described by a Fokker-Planck diffusion model that contained preference behaviour at the interface and did not account for habitat specific motility. Likewise, motility calculated from movement data using the Patlak model was not different between habitats in the arena studies. Motility (m2 d-1) calculated from behavioural data resulted in estimates that were similar to those determined in the field. Thus individual behaviour explained population redistribution in the field qualitatively as well as quantitatively. The findings provide a basis for evaluating movement within and across habitats in complex agricultural landscapes with multiple habitats and habitat interfaces.

Comment on "Invasive harlequin ladybird carries biological weapons against native competitors".

We comment on the implications that Vilcinskas et al. (Reports, 17 May 2013, p. 862) attach to the finding that the exotic, invasive ladybird Harmonia axyridis carries microsporidia to which this species is insensitive but that is lethal to species that are native to the invaded areas. The authors suggest that these microsporidia might serve as "biological weapons" against the native competitors, but we cast doubt on the importance of this suggestion in the field.

Intraguild predation behaviour of ladybirds in semi-field experiments explains invasion success of Harmonia axyridis.

Harmonia axyridis has been introduced as a biological control agent in Europe and the USA. Since its introduction, it has established and spread, and it is now regarded as an invasive alien species. It has been suggested that intraguild predation is especially important for the invasion success of H. axyridis. The aim of this study was to compare the intraguild predation behaviour of three ladybird species (Coccinella septempunctata, Adalia bipunctata, and H. axyridis). Predation behaviour was investigated in semi-field experiments on small lime trees (Tilia platyphyllos). Two fourth-instar larvae placed on a tree rarely made contact during 3-hour observations. When placed together on a single leaf in 23%-43% of the observations at least one contact was made. Of those contacts 0%-27% resulted in an attack. Harmonia axyridis attacked mostly heterospecifics, while A. bipunctata and C. septempunctata attacked heterospecifics as often as conspecifics. In comparison with A. bipunctata and C. septempunctata, H. axyridis was the most successful intraguild predator as it won 86% and 44% of heterospecific battles against A. bipunctata and C. septempunctata respectively, whilst A. bipunctata won none of the heterospecific battles and C. septempunctata won only the heterospecific battles against A. bipunctata. Coccinella septempunctata dropped from a leaf earlier and more often than the other two species but was in some cases able to return to the tree, especially under cloudy conditions. The frequency with which a species dropped did not depend on the species the larva was paired with. The results of these semi-field experiments confirm that H. axyridis is a strong intraguild predator as a consequence of its aggressiveness and good defence against predation from heterospecific species. The fact that H. axyridis is such a strong intraguild predator helps to explain its successful establishment as invasive alien species in Europe and the USA.

Will the Convention on Biological Diversity put an end to biological control?

Will the Convention on Biological Diversity put an end to biological control? Under the Convention on Biological Diversity countries have sovereign rights over their genetic resources. Agreements governing the access to these resources and the sharing of the benefits arising from their use need to be established between involved parties. This also applies to species collected for potential use in biological control. Recent applications of access and benefit sharing principles have already made it difficult or impossible to collect and export natural enemies for biological control research in several countries. If such an approach is widely applied it would impede this very successful and environmentally safe pest management method based on the use of biological diversity. The International Organization for Biological Control of Noxious Animals and Plants has, therefore, created the "Commission on Biological Control and Access and Benefit Sharing". This commission is carrying out national and international activities to make clear how a benefit sharing regime might seriously frustrate the future of biological control. In addition, the IOBC Commission members published information on current regulations and perceptions concerning exploration for natural enemies and drafted some 30 case studies selected to illustrate a variety of points relevant to access and benefit sharing. In this article, we summarize our concern about the effects of access and benefit sharing systems on the future of biological control.

Poderá a Convenção em Diversidade Biológica por um fim no Controle Biológico? Baseando-se na Convenção sobre Diversidade Biológica, os países têm soberania sobre seus recursos genéticos. Acordos que governam o acesso a tais recursos e o compartilhamento dos benefícios provenientes do seu uso precisam ser estabelecidos de comum acordo com as partes envolvidas. Isto também é aplicável a espécies coletadas com uso potencial em controle biológico. Recentes aplicações dos princípios de introdução e compartilhamento dos benefícios têm tornado difícil, ou mesmo impossível, coletar e exportar inimigos naturais em muitos paises para pesquisas em controle biológico em muitos países. Como esta é uma medida amplamente utilizada, tais procedimentos poderão impedir este bem sucedido e ambientalmente seguro método de manejo de pragas, baseado no uso da diversidade biológica. A Organização Internacional para Controle Biológico de Plantas e Animais Nocivos (IOBC) criou a "Comissão em Controle Biológico e Introdução e Benefícios Mútuos" para estudar o assunto. Tal comissão está desenvolvendo atividades nacionais e internacionais para esclarecer como o regime de compartilhamento de benefícios pode prejudicar seriamente o futuro do controle biológico. Além disto, membros da Comissão da IOBC publicaram informações sobre regulamentos atuais e suas opiniões relacionadas à exploração de inimigos naturais, listando cerca de 30 casos para ilustrar os pontos relevantes para a introdução e compartilhamento de benefícios. No presente artigo, é sumarizado o ponto de vista dessa comissão na IOBC sobre os efeitos dos sistemas de introdução e compartilhamento para o futuro do Controle Biológico.

Life history parameters of Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) at different environmental conditions on two bean cultivars.

Life-history parameters of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), an important pest of bean crops in Colombia, were determined in environmental control chambers on two dry bean (Phaseolus vulgaris) cultivars (cv.). Trialeurodes vaporariorum longevity on cv. Chocho decreased as temperature increased from 22.6 d at 19 degrees C to 5.9 d at 26 degrees C. Fecundity was significantly lower at 19 degrees C (8.6 eggs/female), as compared to 22 degrees C (32.6 eggs/female) and 26 degrees C (33.3 eggs/female) on cv. Chocho. Fecundity on cv. ICA-Pijao was much higher (127.2 eggs/female) than on cv. Chocho (32.6 eggs/female) at 19 degrees C. The intrinsic rate of population increase (r m) was highest at 22 degrees C (0.061), intermediate at 19 degrees C (0.044) and lowest at 26 degrees C (0.035) on cv. Chocho, and was 0.072 on cv. ICA-Pijao at 19 degrees C. Life history parameters of T. vaporariorum are compared to those of one of its natural enemies, the parasitoid Amitus fuscipennis MacGown & Nebeker. Finally, data are presented on the distribution of the parasitoid related to the altitude for the Valle del Cauca, Colombia.

Structure and electrophysiological responses of gustatory organs on the ovipositor of the parasitoid Leptopilina heterotoma.

Location, structure and histology of chemosensilla on the tip of the ovipositor of the parasitoid Leptopilina heterotoma are described based on SEM and TEM studies. Furthermore, we developed a method for recording extracellular action potentials from the gustatory neurons in response to host haemolymph. This method allowed us to record multi-unit recordings from a sensillum occurring singly on the unpaired ovipositor valve. The TEM study of the ovipositor tip revealed the presence of six dendrites, the electrophysiological recordings provided evidence for the activity of three or possibly four gustatory neurons in response to the complex stimulus offered, leaving other taste functions or a mechanoreceptor function open for the remaining neurons.

Time allocation of a parasitoid foraging in heterogeneous vegetation: implications for host-parasitoid interactions.

1. Changing plant composition in a community can have profound consequences for herbivore and parasitoid population dynamics. To understand such effects, studies are needed that unravel the underlying behavioural decisions determining the responses of parasitoids to complex habitats. 2. The searching behaviour of the parasitoid Diadegma semiclausum was followed in environments with different plant species composition. In the middle of these environments, two Brassica oleracea plants infested by the host Plutella xylostella were placed. The control set-up contained B. oleracea plants only. In the more complex set-ups, B. oleracea plants were interspersed by either Sinapis alba or Hordeum vulgare. 3. Parasitoids did not find the first host-infested plant with the same speed in the different environments. Sinapis alba plants were preferentially searched by parasitoids, resulting in fewer initial host encounters, possibly creating a dynamic enemy-free space for the host on adjacent B. oleracea plants. In set-ups with H. vulgare, also, fewer initial host encounters were found, but in this case plant structure was more likely than infochemicals to interfere with the searching behaviour of parasitoids. 4. On discovering a host-infested plant, parasitoids located the second host-infested plant with equal speed, demonstrating the effect of experience on time allocation. Further encounters with host-infested plants that had already been visited decreased residence times and increased the tendency to leave the environment. 5. Due to the intensive search of S. alba plants, hosts were encountered at lower rates here than in the other set-ups. However, because parasitoids left the set-up with S. alba last, the same number of hosts were encountered as in the other treatments. 6. Plant composition of a community influences the distribution of parasitoid attacks via its effects on arrival and leaving tendencies. Foraging experiences can reduce or increase the importance of enemy-free space for hosts on less attractive plants.

Enter the matrix: how to analyze the structure of behavior.

Several methods are available for analyzing different aspects of behavioral transition matrices, but a comprehensive framework for their use is lacking. We analyzed parasitoid foraging behavior in environments with different plant species compositions. The resulting complex data sets were analyzed using the following stepwise procedure. We detected abrupt changes in the event log files of parasitoids, using a maximum likelihood method. This served as a criterion for splitting the event log files into two parts. For both parts, Mantel's test was used to detect differences between first-order transition matrices, whereas an iterative proportional fitting method was used to find behavioral flows that deviated from random transitions. In addition, hidden repetitive sequences were detected in the transition matrices on the basis of their relative timing, using Theme. We discuss the results for the example from a biological context and the comprehensive use of the different methods. We stress the importance of such a combined stepwise analysis for detecting differences in some parts of event log files.

Pathogenicity of Aschersonia spp. against whiteflies Bemisia argentifolii and Trialeurodes vaporariorum.

Entomopathogenic fungi of the genus Aschersonia are specific for whitefly and scale insects. They can be used as biological control agents against silverleaf whitefly, Bemisia argentifolii and greenhouse whitefly, Trialeurodes vaporariorum. Forty-four isolates of Aschersonia spp. were tested for their ability to sporulate and germinate on semi-artificial media and to infect insect hosts. Seven isolates sporulated poorly (less than 1x10(7) conidia/dry weight) and 10 were not able to infect either of the whitefly species. Several isolates were able to produce capilliconidia. Infection level was not correlated with germination on water agar. After a selection based on spore production and infection, virulence of 31 isolates was evaluated on third instar nymphs of both whitefly species on poinsettia (Euphorbia pulcherrima). Whitefly infection levels varied between 2 and 70%, and infection percentages of B. argentifolii correlated with that of T. vaporariorum. However, mortality was higher for T. vaporariorum than for B. argentifolii, as a result of a higher 'mortality due to unknown causes.' Several isolates, among which unidentified species of Aschersonia originating from Thailand and Malaysia, A. aleyrodis from Colombia, and A. placenta from India showed high spore production on semi-artificial medium and high infection levels of both whitefly species.