How <Emphasis Type="Italic">Trichogramma</Emphasis> survives during soybean offseason in Southern Brazil and the implications for its success as a biocontrol agent

Trichogramma species are important natural enemies of Anticarsia gemmatalis Hübner, a key pest of soybean in new world agroecosystems. Development, longevity and parasitism rate of Trichogramma pretiosum Riley, Trichogramma acacioi Brun, Moraes and Soares and Trichogramma rojasi Nagaraja and Nagarkatti were investigated under natural conditions throughout fall and winter in order to determine how these parasitoids survive during the soybean off-season in southern Brazil. All species remained active along the experimental period. Over 90 % of the parasitoids emerged throughout the off-season, except for T. rojasi which showed lower percentage of emergence in April and May. The reproductive activity was not interrupted during fall and winter, indicating that the parasitoids depend on alternative hosts to survive. Parasitoids survived during the off-season combining slow developmental rate with an increase in adult life span, an important adaptation that improves their chances of finding alternative hosts and food sources.     

Predators and parasitoids of the harlequin ladybird, <Emphasis Type="Italic">Harmonia axyridis</Emphasis>, in its native range and invaded areas

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) has rapidly spread in several continents over the past 30 years and is considered an invasive alien species. The success of H. axyridis as an invader is often attributed to weak control by natural enemies. In this paper, we provide an overview of current knowledge on predators and parasitoids of H. axyridis. The common feature of predators and parasitoids is that they directly kill exploited organisms. Currently available data show that H. axyridis, displaying a variety of chemical, mechanical, and microbiological anti-predator defenses, is usually avoided by predators. However, some birds and invertebrates can eat this ladybird without harmful consequences. The primary defenses of H. axyridis against parasitoids include immune response and physiological and nutritional unsuitability for parasitoid development. These defenses are probably relatively efficient against most ladybird parasitoids, but not against flies of the genus Phalacrotophora. The latter are idiobiont parasitoids and hence can evade the host’s immune response. Indeed, rates of parasitism of H. axyridis by Phalacrotophora in the Palaearctic region (both in the native range in Asia and in Europe) are relatively high. While strong evidence for enemy release on the invasive populations of H. axyridis is lacking, several cases of parasitoid acquisition have been recorded in Europe, North America, and South America. We conclude that enemy release cannot be excluded as a possible mechanism contributing to the spread and increase of H. axyridis in the early stages of invasion, but adaptation of parasitoids may lead to novel associations which might offset previous effects of enemy release. However, further work is required to elucidate the population-level effects of such interactions.     

Ants visiting extrafloral nectaries and pyrrolizidine alkaloids may shape how a specialist herbivore feeds on its host plants

The presence of extrafloral nectaries (EFNs) attracts predators and parasitoids, and protects the plant against herbivorous insects. By improving plant defences, EFNs reduce the fitness of herbivores. The use of similar host plants with no EFNs or adaptations in response to predators and parasitoids may enhance herbivore fitness. In this context, we studied the feeding habit (on leaves or on unripe seeds inside the pods) of larvae of the specialist moth Utetheisa ornatrix in two Crotalaria host plant species in which EFNs are present (C. micans) or absent (C. paulina). We hypothesized that the moths’ feeding habit was influenced by its natural enemies via their presence on EFNs. In C. micans, we found more larvae feeding inside the pods rather than on the leaves, while in C. paulina, larvae were found in both parts of the plant. There was greater activity of natural enemies in C. micans than in C. paulina. The moth sequesters enough pyrrolizidine alkaloid (PAs) to defend against predators in the leaves and seeds of C. paulina, but only in seeds of C. micans. Therefore, a change in the feeding habit in U. ornatrix larvae is a plastic response that depends on whether EFNs are present or not, or whether PA concentrations are low or high. This change does not affect overall moth performance. However, other factors, such as pod hardness, predation by organisms other than those visiting EFNs or even parasitoids cannot be ruled out as being responsible for the change in feeding habit. To date, both the EFNs and PAs in Crotalaria species are a parsimonious explanation of how larvae of U. ornatrix use different species of Crotalaria for feeding.     

Impact of multiple natural enemies on immature <Emphasis Type="Italic">Drosophila suzukii</Emphasis> in strawberries and blueberries

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) oviposits in ripening fruit, larvae render crops unmarketable, and significant economic losses can occur. Biological control research has focused on individual natural enemy species against immature D. suzukii. Here we combine two predators and an entomopathogenic nematode, expecting species complementarity and increased control of D. suzukii. In strawberries, Orius insidiosus (Say) (Hemiptera: Anthocoridae) plus Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) resulted in fewest D. suzukii (81% reduction), and in blueberries, results were similar (60% reduction), although H. bacteriophora was not as effective as in strawberries, which was likely due to drier substrate conditions. There was neither strong complementarity nor interference between predators, O. insidiosus and Dalotia coriaria Kraatz (Coleoptera: Staphylinidae). Inclusion of O. insidiosus resulted in 50% fewer D. suzukii than combinations without O. insidiosus. Control of D. suzukii can be improved with multiple natural enemies, and combinations of O. insidiosus with other agents (parasitoids, fungal entomopathogens) should be tested.     

A mixture of herbivore-induced plant volatiles from multiple host plant species enhances the attraction of a predatory bug under field-cage conditions

Plants respond to herbivore attack by emitting a blend of volatiles called herbivore-induced plant volatiles (HIPVs), which attract arthropod natural enemies. Under natural conditions and multiple cropping agriculture systems, natural enemies are thought to encounter a mixture of HIPVs emanating from multiple plant species. The effect of such a mixture of HIPVs on the responses of natural enemies under field conditions has not been explored. Our study assessed whether a mixture of HIPVs from multiple host plant species influenced predator responses in field-cage conditions. We investigated (1) foraging behaviors of a predatory bug, Orius strigicollis, on cotton bollworm (Helicoverpa armigera) larvae-infested multiple host plant species, and (2) the attractiveness of a mixture of reconstituted HIPVs from multiple plant species to O. strigicollis in outdoor cages. Significantly, greater numbers of predators were attracted to H. armigera-infested multiple plant species. The predators exterminated significantly greater numbers of H. armigera larvae with the multiple versus single plant species treatments. Significantly, greater numbers of O. strigicollis were captured on traps baited with the mixture of reconstituted HIPVs from multiple versus single plant species. The enhanced attractiveness of a mixture of HIPVs from multiple plant species to O. strigicollis might be the result of an additive effect of HIPVs from the three plant species when combined in a mixture.     

Parasitoids and fungal pathogens of <Emphasis Type="Italic">Phyllonorycter issikii</Emphasis> (Kumata, 1963) from Bulgaria

The lime leaf miner, Phyllonorycter issikii, is a moth species native to East Asia, which recently invaded considerable part of Europe. A study on the natural enemies of this invasive species was conducted in Bulgaria. Tilia cordata leaves infested with the lime leaf miner were collected in 2015 and 2016 in two public parks in Sofia. A total of eleven eulophid parasitoids (Hymenoptera: Eulophidae) belonging to three subfamilies - Entedoninae, Eulophinae and Tetrastichinae, and one braconid species (Hymenoptera: Braconidae) were recorded. In addition, one unidentified ichneumonid species was reared. Minotetrastichus platanellus was the most abundant species in the samples comprising 76.88% of the parasitoids reared from collected immature and pupal stages of Ph. issikii. It is followed by Sympiesis gordius (6.53%) and S. sericeicornis (6.03%). Three new host-parasitoid associations were established. The entomopathogenic fungi Beuveria bassiana and Metarhizium anisopliae (Hypocreales) were isolated for the first time from cadavers of Ph. issikii larvae and pupae. Based on the presented observation we hypothesized that the lime leaf miner can produce three generations in Bulgaria.     

Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles

Plants damaged by herbivores emit blends of volatile organic compounds (VOCs) that attract the herbivore’s natural enemies. Most work has focussed on systems involving one plant, one herbivore and one natural enemy, though, in nature, plants support multiple herbivores and multiple natural enemies of these herbivores. Our study aimed to understand how different aphid natural enemies respond to aphid-induced VOCs, and whether attraction of the natural enemies that responded to aphid-induced VOCs was altered by simultaneous damage by a chewing herbivore. We used a model system based on Brassica juncea (Brassicaceae), Myzus persicae (Hemiptera: Aphididae) and Plutella xylostella (Lepidoptera: Plutellidae). Ceraeochrysa cubana (Neuroptera: Chrysopidae) did not show preferences for any plant odour, while Cycloneda sanguinea (Coleoptera: Coccinellidae) responded to undamaged plants over air but not to aphid-damaged plants over undamaged plants. Therefore, no further tests were carried out with these two species. Chrysoperla externa (Neuroptera: Chrysopidae) preferred aphid-damaged plants, but not caterpillar-damaged plants, over undamaged plants, and preferred plants damaged by both herbivores over both undamaged plants and aphid-damaged plants. When tested for responses against undamaged plants, Aphidius colemani (Hymenoptera: Braconidae) preferred aphid-damaged plants but not plants damaged by caterpillars. Plants damaged by both herbivores attracted more parasitoids than undamaged plants, but not more than aphid-damaged plants. Thus, multiply damaged plants were equally attractive to A. colemani and more attractive to C. externa than aphid-damaged plants, while C. cubana and C. sanguinea did not respond to aphid-induced VOCs, highlighting how different natural enemies can have different responses to herbivore-damaged plants.     

Feasibility assessment for the classical biological control of <Emphasis Type="Italic">Tamarix</Emphasis> in Argentina

Saltcedars are woody plants in the genus Tamarix L. (Caryophyllales: Tamaricaceae) and are native to Eurasia and Africa. Several species have become invasive in the Americas, Australia and South Africa. In Argentina there are four species of Tamarix distributed in arid, semi-arid and coastal areas of most provinces. The taxonomic isolation of Tamarix spp. in Argentina, their widespread distribution, negative impact to natural areas and lack of impact from existing natural enemies all indicate that Tamarix is an ideal candidate for classical biological control in Argentina. Biological control of Tamarix spp. has been rapid and highly successful in the USA after the introduction of four Diorhabda spp. (Coleoptera: Chrysomelidae). Biological control of Tamarix spp. in Argentina could be implemented easily, rapidly, and at a low cost by utilizing the information developed in the USA.     

<Emphasis Type="Italic">Bactrocera oleae</Emphasis> pupae predation by <Emphasis Type="Italic">Ocypus olens</Emphasis> detected by molecular gut content analysis

The pupae of Bactrocera oleae (Diptera: Tephritidae) complete their development during autumn and winter in the soil, rather than in the drupe, resulting susceptible to edaphic predators. Environmentally friendly methods to control this olive pest involve the identification of its natural enemies. This study evaluated the role of Ocypus olens (Coleoptera: Staphylinidae) in the predation of B. oleae pupae, by means of molecular gut content analysis. Modified dry pitfall traps were used to collect live specimens from low-input olive orchards in Tuscany (Italy). Sampling was fine-tuned with a degree-day model estimating the presence of pest pupae in the soil. PCR analyses carried out on field-collected specimens demonstrated that O. olens is a predator of B. oleae, at least during autumn. These results are consistent with predictions of the degree-day model. Knowledge on species composition, traits and complementarity of the natural enemies of B. oleae pupae needs further investigation to advance conservation biological control strategies.     

Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (<Emphasis Type="Italic">Brassica napus</Emphasis>) crops

Reducing the use of insecticides is an important issue for agriculture today. Sowing wildflower strips along field margins or within crops represents a promising tool to support natural enemy populations in agricultural landscapes and, thus, enhance conservation biological control. However, it is important to sow appropriate flower species that attract natural enemies efficiently. The presence of prey and hosts may also guide natural enemies to wildflower strips, potentially preventing them from migrating into adjacent crops. Here, we assessed how seven flower traits, along with the abundance of pollen beetles (Meligethes spp., Coleoptera: Nitidulidae) and true weevils (Ceutorhynchus spp., Coleoptera: Curculionidae), affect the density of parasitoids of these two coleopterans in wildflower strips sown in an oilseed rape field in Gembloux (Belgium). Only flower traits, not host (i.e. pollen beetles and true weevils) abundance, significantly affected the density of parasitoids. Flower colour, ultraviolet reflectance and nectar availability were the main drivers affecting parasitoids. These results demonstrate how parasitoids of oilseed rape pests react to flower cues under field conditions. Similar analyses on the pests and natural enemies of other crops are expected to help to develop perennial flower mixtures able to enhance biological control throughout a rotation system.     

Carabid patterns in olive orchards and woody semi-natural habitats: first implications for conservation biological control against <Emphasis Type="Italic">Bactrocera oleae</Emphasis>

The role of carabids (Coleoptera: Carabidae) for pest control service in perennial crop systems has been scarcely investigated. We addressed this knowledge gap exploring activity patterns and traits of adult carabids dwelling olive orchard agroecosystems as potential natural enemies of third instar larvae and pupae of Bactrocera oleae (Diptera: Tephritidae). Olive orchard supported a well-structured carabid assemblage, whose species phenologies revealed a temporal overlapping within the pest cycle. The assemblage of adjacent woody semi-natural habitats is more of conservation interest, but may play a weaker role in B. oleae control provisioning. We suggest the identification of carabids main traits for B. oleae conservation biological control as a cost-effective strategy for addressing future attention and resources only to those predators that satisfy basic requirements. This research may open new scenarios on management interventions to both conserve predators and encourage alternative approaches against olive orchards pest.     

The impact of ant attendance on protecting <Emphasis Type="Italic">Aphis gossypii</Emphasis> against two aphidophagous predators and it’s role on the Intraguild Predation between them

In this study the changes in Aphis gossypii Glover populations tended by the homopteran- tending ant, Tapinoma simrothi Krausse when exposed to the natural enemies Chrysoperla carnea Stephens and Coccinellia septempunctata Mulsant was studied. We also studied the effect of ant’s attendance on the consequence of intraguild predation (IGP) between these two predators. The presence of ants T. simrothi had deterrent impact on natural enemies of A. gossypii compared to control aphid populations in absence of ants. Equally we observed that IGP between two aphid predators decreased when T. simrothi was present. The lowest IGP level was observed when both aphids and ants were present in the microcosm arena. In the microcosm arena the presence of ants had an indirect effect on the occurrence of IGP. Our results suggest that although the mutualistic ants have an indirect impact on the IGP by aphidophages predators, but their roles should not be ignored.     

Responses of a predatory bug to a mixture of herbivore-induced plant volatiles from multiple plant species

The attractiveness of herbivore-induced plant volatiles (HIPVs) from a specific plant species to natural enemies has been well established. However, under natural conditions and polycultural agriculture systems, the interactions among trophic levels are thought to be more complex. For instance, complex mixtures of volatiles emitted from diverse host plant species infested by polyphagous herbivores might affect responses of natural enemies. In this study, we investigated whether a mixture of HIPVs emitted from herbivore-damaged multiple host plant species affect responses of a predatory bug. Therefore, we report (1) olfactory responses of the predatory bug (Orius strigicollis) to volatiles emitted from cotton bollworm (Helicoverpa armigera) first instar larvae-damaged multiple plant species (tomato, French bean and sweet corn), (2) chemical analyses of volatiles emitted from the three plant species exposed to different treatments and (3) olfactory responses of the predators to a reconstituted HIPV blend from multiple plant species based on chemical analyses. O. strigicollis significantly preferred volatiles emanating from H. armigera-damaged multiple plant species to volatiles emanating from a single plant species. In all the three plant species, H. armigera-damaged seedlings emitted significantly a greater amount of volatiles as well as a larger number of volatile compounds than an undamaged or a mechanically injured seedling. The predators preferred the reconstituted HIPVs from multiple plant species to the reconstituted HIPVs from a single plant species. Thus, the mixture of HIPVs from multiple plant species enhanced the attractiveness to the predators.     

On distribution and ecology of some species of cleonines (Coleoptera,Curculionidae): IV. Genus <Emphasis Type="Italic">Lixus</Emphasis> F., subgenus <Emphasis Type="Italic">Eulixus</Emphasis> Reitt.

Data on habitats, food plants of larvae and adults, feeding, mating, oviposition, larval and pupal development, natural enemies, and distribution of seven weevil species (Lixus canescens F.-W., L. iridis Ol., L. myagri Ol., L. punctirostris Boh., L. subtilis Boh., L. incanescens Boh., and L. brevipes Bris.) are given. New host plants of L. canescens and L. iridis are revealed. Gall induction by L. brevipes is reported for the first time. Distribution of all the species in Ukraine and Russia (the latter based on the literature) are given in more detail. Information on the known and potential economic importance of every species is provided.     

Ants Do Not Traverse the Silk of Adult Female <Emphasis Type="Italic">Nephila clavipes</Emphasis> (Linnaeus) Webs

Many organisms use chemicals to deter enemies. Some spiders can modify the composition of their silk to deter predators from climbing onto their webs. The Malaysian golden orb-weaver Nephila antipodiana (Walckenaer) produces silk containing an alkaloid (2-pyrrolidinone) that functions as a defense against ant invasion—ants avoid silk containing this chemical. In the present study, we test the generality of ants’ silk avoidance behavior in the field. We introduced three ant species to the orb webs of Nephila clavipes (Linnaeus) in the tropical rainforest of La Selva, Costa Rica. We found that predatory army ants (Eciton burchellii Westwood) as well as non-predatory leaf-cutting ants (Atta cephalotes Linnaeus and Acromyrmex volcanus Wheeler) avoided adult N. clavipes silk, suggesting that an additional species within genus Nephila may possess ant-deterring silk. Our field assay also suggests that silk avoidance behavior is found in multiple ant species.     

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.     

Supplemental releases of specialist parasitic wasps improve whitefly and psyllid control by <Emphasis Type="Italic">Dicyphus hesperus</Emphasis> in tomato

Dicyphus hesperus Knight (Heteroptera: Miridae) can contribute to the suppression of populations of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and Bactericera cockerelli Sulcer (Hemiptera: Psyllidae) in tomato. Nevertheless, the remaining levels of these pests could still be too high for the crop to tolerate. We thus tested here whether the combination of D. hesperus with the specialist parasitoids Eretmocerus eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae) (whitefly) and Tamarixia triozae (psyllid) can result in better pest control compared with methods based exclusively on single-species releases in tomato. We conducted two simultaneous experiments in tomato (‘Whitefly’ and ‘Psyllid’ Experiment), where we compared the effectiveness against B. tabaci and B. cockerelli in cages receiving releases of the predator or the specialist parasitoid alone, or in combination. Although all natural enemies reduced pest levels when released separately, the combination of D. hesperus with E. eremicus and D. hesperus with T. triozae resulted in better whitefly and psyllid control, respectively, compared with the separate releases.     

Assessing the distribution and conservation status of a long-horned beetle with species distribution models

Data shortfalls on species distribution affect species differently, but it is frequent among insects. Species distribution models (SDMs) are important tools to fill biogeographic deficits and provide support for practical conservation actions, particularly for cryptic or hard to survey species. We employed SDMs to evaluate one such species, the long-horned beetle (Macrodontia cervicornis), listed as ‘vulnerable’ in the IUCN’s Red List of Threatened Species. Given new distributional data for this species, we applied three different SDMs to: (1) provide the first assessment of this species’ distribution and potential dispersal routes; (2) evaluate the effectiveness of the current South American protected areas system for its conservation; and (3) discuss its potential distribution, as well as historical, biogeographical, and taxonomic issues related to it. Our models reached fair True Skilled Statistics values (TSS > 0.5), with the core area for M. cervicornis located in the Amazon forest, although suitable areas were also predicted along the Atlantic forest. Areas in the dry diagonal South American corridor (dry biomes of Cerrado, Caatinga, and Pampas) in South America were not predicted as suitable. The preference of M. cervicornis for humid areas with high temperatures may guarantee a better physiological control for dehydration, considering that large insects are more affected by water loss. In general, approximately 15 % of the distribution of M. cervicornis is in humid protected areas. The disconnected distribution of the long-horned beetle may be an indication of the existence of cryptic species under the same classification. We suggest that similar studies with other insect groups (e.g. butterflies, bees) should be conducted to properly assess their distributions, conservation status, and responses to hot-humid gradients throughout South America.     

Spatio-temporal variation of strawberry aphid populations and their parasitoids

Aphids are common herbivores in the strawberry crop that can reduce plant vigor and fruit quality and also transmit viruses. Aphid species prefer diverse plant organs, which represent particular habitats of different quality for aphids and for the development of natural enemies’ populations. Different habitat units (young leaves, mature leaves, buds, flowers) of strawberry were sampled fortnightly during all seasons. We identified seven aphid species, namely Chaetosiphon fragaefolii, Aphis gossypii, and Macrosiphum euphorbiae, the most abundant. During the autumn, C. fragaefolli and M. euphorbiae were scarce and A. gossypii was denser on mature leaves, while during summer M. euphorbiae was absent. During the winter, C. fragaefolii predominated on buds and young leaves, A. gossypii on flowers, and both species on mature leaves. During the spring, C. fragaefolii was even more abundant on buds, A. gossypii predominated on mature leaves, and the three species were equally abundant on flowers and young leaves. Parasitoids emerged from A. gossypii, M. euphorbiae and Myzus persicae, but not from C. fragaefolii. Three Aphidius and two Aphelinus species were recovered. All primary parasitoid species emerged from A. gossypii, and secondary parasitoids emerged only from this aphid. Aphis gossypii parasitism on mature leaves was markedly higher in winter and summer than in autumn and spring. Parasitism of A. gossypii was independent of its density, and the number of parasitized aphids was never higher than six. Our results contribute to define the most appropriate sample unit to estimate aphid density of different species and provide information about seasonal natural parasitism.     

Acorns of invasive Northern Red Oak (<Emphasis Type="Italic">Quercus rubra</Emphasis>) in Europe are larval hosts for moths and beetles

In their first phase of expanding into new areas, invasive plants often take advantage of the inability of existing herbivores and pathogenic species to exploit them. However, in the longer term local enemies may adapt to using these invasive species as a food source. This study assesses the use of mature acorns of two oak species in Europe (the native Pedunculate Oak Quercus robur and the invasive Northern Red Oak Quercus rubra) by moths Cydia fagiglandana and Cydia splendana and beetles Curculio spp. We show that acorns of invasive oak species can be equally attractive to C. splendana but only partially so to C. fagiglandana where infestation rates where significantly lower (approximately half) compared to the native oak. The infestation by Curculio beetles of Northern Red Oak was marginal, less than 1% of the rate in the native oak species. The larval final weights did not differ significantly between host species, but emergence of C. splendana and Curculio spp. took significantly longer in acorns of Northern Red Oak. It is likely that C. fagiglandana and C. splendana have increased their niche breadths by exploiting invasive oak species and avoiding competition with the Curculio weevils. Furthermore, the occurrence of Northern Red Oak could stabilize food resources during years when native oak species have poor acorn crops.