Compatibility of two predator species for biological control of the two-spotted spider mite.

Because predators may interfere with each other, an important step towards the implementation of successful release of multiple predators in biocontrol programs requires resolving how predators respond to the presence of heterospecific competitors. Several species of predatory mites are important biocontrol agents and the species Phytoseiulus macropilis and Neoseiulus californicus are used to control the two-spotted spider mite, Tetranychus urticae, an important pest in agriculture worldwide. We investigated their compatibility showing that the two predators do not avoid plants on which the other species is present together with their common prey, and demonstrated that their oviposition rates are not affected by the presence of the other species. However, the distribution of the eggs on leaf discs was affected by the presence of the heterospecific predator. This behaviour might weaken possible interference between these two biocontrol agents, which, in turn, may enable their persistence on plants and favour pest suppression. The increased joint use of several natural enemies for biological control highlights the importance of studies on predator-predator interactions.

Ontogenetic stage-specific reciprocal intraguild predation.

The size or stage of interacting individuals is known to affect the outcome of ecological interactions and can have important consequences for population dynamics. This is also true for intraguild predation (the killing and eating of potential competitors), where the size or ontogenetic stage of an individual determines whether it is the intraguild predator or the intraguild prey. Studying size- or stage-specific interactions is therefore important, but can be challenging in species with complex life histories. Here, we investigated predatory interactions of all feeding stages of the two predatory mite species Neoseiulus californicus and Phytoseiulus macropilis, both of which have complex life cycles, typical for predatory arthropods. Populations of these two species compete for two-spotted spider mites, their prey. We evaluated both the capacity to kill stages of the other predator species and the capacity to benefit from feeding on these stages, both prerequisites for the occurrence of intraguild predation. Ontogeny played a critical role in the occurrence of intraguild predation. Whereas the juveniles of P. macropilis developed from larva until adulthood when feeding on N. californicus eggs, interestingly, adult female P. macropilis did not feed on the smaller stages of the other species. We furthermore show that intraguild predation was reciprocal: both juveniles and adult females of N. californicus preyed on the smallest stages of P. macropilis. These results suggest that a proper analysis of the interactions between pairs of species involved in intraguild predation should start with an inventory of the interactions among all ontogenetic stages of these species.

Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance.

The outcome of plant-mediated interactions among herbivores from several feeding guilds has been studied intensively. However, our understanding on the effects of nematode root herbivory on leaf miner oviposition behavior and performance remain limited. In this study, we evaluated whether Meloidogyne incognita root herbivory affects Tuta absoluta oviposition preference on Solanum lycopersicum plants and the development of the resulting offspring. To investigate the M. incognita-herbivory induced plant systemic responses that might explain the observed biological effects, we measured photosynthetic rates, leaf trypsin protease inhibitor activities, and analyzed the profile of volatiles emitted by the leaves of root-infested and non-infested plants. We found that T. absoluta females avoided laying eggs on the leaves of root-infested plants, and that root infestation negatively affected the pupation process of T. absoluta. These effects were accompanied by a strong suppression of leaf volatile emissions, a decrease in photosynthetic rates, and an increase in the activity of leaf trypsin protease inhibitors. Our study reveals that root attack by nematodes can shape leaf physiology, and thereby increases plant resistance.

A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) reduces growth and increases secondary metabolite biosynthesis in herbivore-attacked plants.

Plant invertases are sucrolytic enzymes that are essential for the regulation of carbohydrate metabolism and source-sink relationships. While their activity has been well documented during abiotic and biotic stresses, the role of proteinaceous invertase inhibitors in regulating these changes is unknown. Here, we identify a putative Nicotiana attenuata cell wall invertase inhibitor (NaCWII) which is strongly up-regulated in a jasmonate (JA)-dependent manner following simulated attack by the specialist herbivore Manduca sexta. To understand the role of NaCWII in planta, we silenced its expression by RNA interference and measured changes in primary and secondary metabolism and plant growth following simulated herbivory. NaCWII-silenced plants displayed a stronger depletion of carbohydrates and a reduced capacity to increase secondary metabolite pools relative to their empty vector control counterparts. This coincided with the attenuation of herbivore-induced CWI inhibition and growth suppression characteristic of wild-type plants. Together our findings suggest that NaCWII may act as a regulatory switch located downstream of JA accumulation which fine-tunes the plant's balance between growth and defense metabolism under herbivore attack. Although carbohydrates are not typically viewed as key factors in plant growth and defense, our study shows that interfering with their catabolism strongly influences plant responses to herbivory.

Molecular markers as a method to evaluate the movement of Hypothenemus hampei (Ferrari).

The objective of this research was to develop a methodology to describe the movement of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae) in the field through: (i) the evaluation of allele variation of a microsatellite marker on polymorphic Colombian H. hampei populations; (ii) the invention of a device for releasing H. hampei adults; (iii) the standardization of a release-recapture technique for H. hampei populations; (iv) the estimation of the flight distance of the insect; and (v) the calculation of a mathematical expression that describes the movement of H. hampei in space over time. The results indicated that: (i) the microsatellite molecular marker HHK.1.6 was exclusively present in a population from Guapotá-Santander, was dominant and allows the evaluation of H. hampei movement for several generations; (ii) a device that released 88.8% of H. hampei adults in 2 s was designed; (iii) this device was used as H. hampei populations containing HHK.1.6 marker release strategy, and coffee seeds as recapture strategy; (iv) it was estimated that H. hampei adults flew as far as 65 m, however, 90% were recovered in a radius of <40 m. Finally, (v) the mathematical expression that described the movement of H. hampei in space over time was [Formula: see text], being [Formula: see text] the average number of borer beetles recaptured per tree, and x the distance in meters. This method will allow to determine the movement of H. hampei from different environmental and ecological scenarios.

Attracted to the enemy: Aedes aegypti prefers oviposition sites with predator-killed conspecifics.

Oviposition habitat choices of species with aquatic larvae are expected to be influenced by both offspring risk of mortality due to predation, and offspring growth potential. Aquatic predators may indirectly influence growth potential for prey by reducing prey density and, for filter-feeding prey, by increasing bacterial food for prey via added organic matter (feces, partially eaten victims), creating the potential for interactive effects on oviposition choices. We tested the hypothesis that the mosquito Aedes aegypti preferentially oviposits in habitats with predatory Toxorhynchites larvae because of indirect effects of predation on chemical cues indicating bacterial abundance. We predicted that A. aegypti would avoid oviposition in sites with Toxorhynchites, but prefer to oviposit where bacterial food for larvae is abundant, and that predation by Toxorhynchites would increase bacterial abundances. Gravid A. aegypti were offered paired oviposition sites representing choices among: predator presence; the act of predation; conspecific density; dead conspecific larvae; and bacterial activity. A. aegypti preferentially oviposited in sites with Toxorhynchites theobaldi predation, and with killed conspecific larvae, but failed to detect preferences for other treatments. The antibiotic tetracycline eliminated the strongest oviposition preference. Both predation by Toxorhynchites and killed larvae increased bacterial abundances, suggesting that oviposition attraction is cued by bacteria. Our results show the potential for indirect effects, like trophic cascades, to influence oviposition choices and community composition in aquatic systems. Our results suggest that predators like Toxorhynchites may be doubly beneficial as biocontrol agents because of the attraction of ovipositing mosquitoes to bacterial by-products of Toxorhynchites feeding.

Determining Factors and Economic Injury Levels for Sphenophorus levis for Chemical and Biological Control in Irrigated and Non-irrigated Sugarcane Crops.

Globally, people use sugarcane (Saccharum officinarum) to produce sugar and ethanol. Rainfed or irrigated sugarcane agricultural systems are available. Among the pests affecting this crop, the weevil Sphenophorus levis, Vaurie 1978 (Coleoptera: Curculionidae), is increasingly becoming a significant threat in southern South America. Sphenophorus levis populations are controlled using chemical or biological measures. Control decisions hinge upon the economic injury level (EIL). The EIL delineates the pest density that results in financial losses for producers. This study aims to determine the EIL for S. levis, considering the factors favoring this insect pest and chemical and biological control methods in rainfed and irrigated systems. The intensity of S. levis attacks was monitored in commercial sugarcane plantations over four years in João Pinheiro, Minas Gerais, Brazil. Sampling occurred in a 50 × 50 × 30-cm-deep trench dug in the soil surrounding the sugarcane clump. The total number of stumps in the clump, including those attacked by S. levis, was tallied. The EILs for this pest were 5.93% and 4.85% of targeted stumps for chemical control in rainfed and irrigated crops, respectively. Biological control in sugarcane plots resulted in an EIL of 4.15% and 3.40% for stumps attacked in rainfed and irrigated crops, respectively. Pest attacks were more severe during rainy years and in older sugarcane crops. The EIL values determined in this study could inform integrated pest management programs for sugarcane crops.

Economic Injury Levels and Economic Thresholds for Leucoptera coffeella as a Function of Insecticide Application Technology in Organic and Conventional Coffee (Coffea arabica), Farms.

Leucoptera coffeella (Lepidoptera: Lyonetiidae) is one of the main pests in coffee crops. The economic injury level (EIL) is the lowest density of the pest at which economic damages match the costs of control measures. The economic threshold (ET) is the density of the pest at which control measures must be taken so that this population does not reach the EIL. These are the main indices used for pest control decision-making. Control of L. coffeella is carried out by manual, tractor, airplane or drone applications. This work aimed to determine EILs and ETs for L. coffeella as a function of insecticide application technology in conventional and organic Coffea arabica crops. Data were collected over five years in commercial C. arabica crops on seven 100 ha central pivots. The cost of control in organic crops was 16.98% higher than conventional. The decreasing order of control cost was manual > drone > airplane > tractor application. Coffee plants were tolerant to low densities (up to 15% mined leaves) of the pest that caused losses of up to 6.56%. At high pest densities (54.20% mined leaves), losses were high (85.62%). In organic and conventional crops and with the use of different insecticide application technologies, EIL and ET were similar. The EIL and ET were 14% and 11% of mined leaves, respectively. Therefore, these indices can be incorporated in integrated pest management programs in C. arabica crops. The indices determined as a function of insecticide application technology in organic and conventional coffee are important as they serve producers with different technological levels. Additionally, EILs and ETs can contribute to more sustainable production, as control methods will only be employed when the pest density reaches these indices.

Development of the spittlebug Mahanarva fimbriolata under varying photophase conditions.

The effects of varying photophase conditions on biological parameters of Mahanarva fimbriolata (Stal) (Hemiptera: Cercopidae), nymphs and adults were evaluated. Eggs of a late developmental stage were placed near sugarcane roots (cultivar RB739735) maintained in a greenhouse (21 ± 7 °C, 90 ± 10% RH). Nymphs and adults were exposed to the following photophase conditions: (a) 13:11 L:D as nymphs and adults, (b) 13:11 as nymphs and 12:12 as adults, (c) 12:12 as nymphs and adults, and d) 12:12 as nymphs and 13:11 as adults. Exposure of nymphs to 13 hr of light significantly reduced the duration of the nymphal stage and the number of nymphs that matured to adults. The duration of the nymphal stage was longer in individuals developing into females than in those developing into males. There was an increase in the longevity of adults kept at 13 hr of light since the nymphal stage. The average longevity of adult males and females was approximately the same. The sex ratio was similar under all photophase conditions. The life cycle of insects kept at 12 and 13 hr of light during nymphal and adult stages respectively was extended. The total life cycle was significantly longer in M. fimbriolata females than males. The different photophase conditions did not affect the reproductive potential of M. fimbriolata. Females produced more diapausing than non-diapausing eggs, except when under 13- and 12-hr light conditions. There was no significant difference in the number of diapausing and non-diapausing eggs produced by females under the other photophase conditions.

The Effect of Resistance to Bt Corn on the Reproductive Output of Spodoptera frugiperda (Lepidoptera: Noctuidae).

The fall armyworm (FAW) Spodoptera frugiperda is the most significant lepidopteran corn pest in South American countries. Transgenic Bt corn, producing the Cry1Fa toxins, has been used to control this pest, but there is clear evidence that some FAW populations have developed resistance. To determine if there are costs associated with resistance, we compared the mass of adults, the duration of mating, and the mass of the first spermatophore produced, as well as the lifetime fecundity and fertility of once-mated susceptible (SS) and resistant (RR) females. Adult mass was affected by both sex and strain, with SS females being significantly larger than RR ones, while the inverse was true for males. RR pairs took significantly longer to mate than SS pairs, yet the mass of spermatophores produced by RR males was significantly less than those of SS males. The total number of eggs laid did not differ but the fertility of eggs from once-mated RR pairs was significantly lower than that of SS pairs. Our data provided clear evidence that the development of Bt resistance affected the reproductive capacity of resistant FAW.

A herbivore that manipulates plant defence.

Phytopathogens and herbivores induce plant defences. Whereas there is evidence that some pathogens suppress these defences by interfering with signalling pathways involved in the defence, such evidence is scarce for herbivores. We found that the invasive spider mite Tetranychus evansi suppresses the induction of the salicylic acid and jasmonic acid signalling routes involved in induced plant defences in tomato. This was reflected in the levels of inducible defence compounds, such as proteinase inhibitors, which in mite-infested plants were reduced to even lower levels than the constitutive levels in herbivore-free plants. Additionally, the spider mite suppressed the release of inducible volatiles, which are implicated in plant defence. Consequently, the mites performed much better on previously attacked plants than on non-attacked plants. These findings provide a new perspective on plant-herbivore interactions, plant protection and plant resistance to invasive species.

Attraction and oviposition of Tuta absoluta females in response to tomato leaf volatiles.

The tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) is a devastating pest of cultivated tomato Solanum lycopersicum throughout South and Central America and Europe. We aimed to characterize the behavioral mechanisms and the chemical cues involved in host selection of T. absoluta females by chemical analysis of tomato leaf volatiles, wind tunnel attraction assays, and oviposition bioassays. Tomato leaf odor elicited in mated females upwind orientation flight followed by landing as well as egg-laying, demonstrating the essential role of plant volatiles in T. absoluta host-finding behavior. In wind tunnel and oviposition choice experiments, T. absoluta females significantly preferred tomato S. lycopersicum over wild tomato Solanum habrochaites, which is resistant to larval feeding. This indicates that leaf volatiles provide information on the suitability of plants as larval hosts. Mated females also discriminated three cultivars of S. lycopersicum according to their volatile profiles. Headspace collections from leaves of these three cultivars contained large amounts of ß-phellandrene, followed by limonene, 2-carene, and (E)-ß-caryophyllene, which together accounted for more than 70% of tomato foliage headspace. Most leaf volatiles were released by all three cultivars, but they showed significant differences with respect to the presence of a few minor compounds and blend proportion. This is an initial study of the volatile signatures that mediate attraction and oviposition of tomato leafminer T. absoluta in response to its main host, tomato.

The dear enemy effect drives conspecific aggressiveness in an Azteca-Cecropia system.

Territoriality is costly, and the accurate identification of intruders and the decision to perform aggressive responses are key behavioral traits in social animals. We studied aggression among individuals belonging to close and distant nests of the plant-ant Azteca muelleri, which lives in stems of the pioneer tree Cecropia glaziovii. More specifically, we aim to investigate if the DE (dear-enemy effect-less aggression towards neighbors than strangers) or NN (nasty-neighbor effect-less aggression to strangers than neighbors) effects or even none of them apply for this iconic Azteca-Cecropia system. We further checked if ant aggression towards conspecifics is related to cuticular hydrocarbon profiles (CHCs), which provide chemical cues for nestmate recognition. Therefore, we sampled 46 nests of A. muelleri in three Brazilian Atlantic forest fragments and performed behavioral trials within and between sites. Consistently with the DE effect, we found higher aggression levels in 'between sites' versus 'within sites' treatments as well as a positive effect of spatial distance on ant aggressiveness. We found no effect of the overall dissimilarities on CHC blend on ant aggressiveness, but of one CHC class, the methylated alkanes. Overall, we provide key insights on nest-mate recognition in obligatory ant-plant mutualisms.

Insecticide toxicity to Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) females and effect on descendant generation.

The effect of nine insecticides used in tomato production was evaluated on adults of two Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) populations from Rive and Afonso Cláudio, Espírito Santo State, Brazil. The experiment was developed in an acclimatized chamber at 25 +/- 1 degrees C, 70 +/- 10% relative humidity and 14 h photophase. Eggs of Anagasta kuehniella (Lepidoptera: Pyralidae), previously immersed in insecticides solutions were offered to females of both T. pretiosum populations. Bacillus thuringiensis, lufenuron and triflumuron had lowest negative effects on parasitism and viability of individuals of these populations; however, abamectin and pyrethroids (betacyflurin 50 and 125 g/l and esfenvalerate) insecticides reduced parasitism rates. T. pretiosum emerged from A. kuehniella eggs treated with esfenvalerate but were not able to parasitize non treated eggs of this host. B. thuringiensis, lufenuron and triflumuron may be used in integrated pest management programs to control tomato pests, because they have moderated negative effect on parasitoid wasps.

The Rolling of Food by Dung Beetles Affects the Oviposition of Competing Flies.

Flies are the main competitors of dung beetles for oviposition sites and rolling dung beetles relocate their food to reduce interspecific competition. Furthermore, dung beetles deposit chemical substances on the food ball that may repel fly larvae and certain predators. In the present study, using Deltochilum furcatum, a dung beetle that does not exhibit parental care and the blow-fly, Lucilia cuprina, we tested the hypothesis that pygidial secretions deposited on the food ball could also make it less attractive as an oviposition site for flies. Food balls rolled by either D. furcatum males or females received significantly fewer eggs that balls that had not been rolled by beetles. Also, flies laid significantly fewer eggs on food balls treated with secretions collected from male pygidial glands. Reduced fly oviposition may be a direct effect of compounds the beetles deposited, acting as an allomone, and/or an indirect negative effect on the microbial community that stimulates fly oviposition. A model of the reproductive biology of this species is proposed.

Queen adoption in colonies of the leaf-cutting ant Acromyrmex subterraneus molestans (Hymenoptera: Formicidae).

Bioassays were conducted in both laboratory and the field to determine if monogynous colonies of Acromyrmex subterraneus molestans (Myrmicinae, Attini) adopt queens from other colonies of the same subspecies. The results suggest that the adoption of fertilized queens is a possible mechanism to explain the occurrence of colonies with multiple queens in this subspecies. Only minor workers were able to discriminate queens from other colonies and were aggressive toward them. Therefore, queen recognition differs among subcastes.

Mutual use of trail-following chemical cues by a termite host and its inquiline.

Termite nests are often secondarily inhabited by other termite species ( = inquilines) that cohabit with the host. To understand this association, we studied the trail-following behaviour in two Neotropical species, Constrictotermes cyphergaster (Termitidae: Nasutitermitinae) and its obligatory inquiline, Inquilinitermes microcerus (Termitidae: Termitinae). Using behavioural experiments and chemical analyses, we determined that the trail-following pheromone of C. cyphergaster is made of neocembrene and (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol. Although no specific compound was identified in I. microcerus, workers were able to follow the above compounds in behavioural bioassays. Interestingly, in choice tests, C. cyphergaster prefers conspecific over heterospecific trails while I. microcerus shows the converse behaviour. In no-choice tests with whole body extracts, C. cyphergaster showed no preference for, while I. microcerus clearly avoided heterospecific trails. This seems to agree with the hypothesis that trail-following pheromones may shape the cohabitation of C. cyphergaster and I. microcerus and reinforce the idea that their cohabitation is based on conflict-avoiding strategies.

Two's a crowd: phenotypic adjustments and prophylaxis in Anticarsia gemmatalis larvae are triggered by the presence of conspecifics.

Defence from parasites and pathogens involves a cost. Thus, it is expected that organisms use this only at high population densities, where the risk of pathogen transmission may be high, as proposed by the "density-dependent prophylaxis" (DDP) hypothesis. These predictions have been tested in a wide range of insects, both in comparative and experimental studies. We think it pertinent to consider a continuum between solitarious and gregarious living insects, wherein: (1) solitarious insects are those that are constitutively solitary and do not express any phenotypic plasticity, (2) the middle of the continuum is represented by insects that are subject to fluctuations in local density and show a range of facultative and plastic changes; and (3) constitutively gregarious forms live gregariously and show the gregarious phenotype even in the absence of crowding stimuli. We aimed to chart some of the intermediary continuum with an insect that presents solitarious aspects, but that is subject to fluctuations in density. Thus, Anticarsia gemmatalis (Lepidoptera: Noctuidae) larvae reared at higher densities showed changes in coloration, a greater degree of encapsulation, had higher hemocyte densities and were more resistant to Baculovirus anticarsia, but not to Bacillus thuringiensis. Meanwhile, with increased rearing density there was reduced capsule melanization. Hemocyte density was the only variable that did not vary according to larval phenotype. The observed responses were not a continuous function of larval density, but an all-or-nothing response to the presence of a conspecific. As A. gemmatalis is not known for gregarious living, yet shows these density-dependent changes, it thus seems that this plastic phenotypic adjustment may be a broader phenomenon than previously thought.

The metasternal and Brindley's glands of Triatoma brasiliensis Neiva (Hemiptera: Reduviidae).

Triatoma brasiliensis Neiva is the most important vector of the Chagas' disease in the semiarid zones of North-eastern Brazil. Adult bugs have two main pairs of exocrine glands, the metasternal and the Brindley's glands, which release volatiles possibly with defense, alarm and/or mating functions. To date, anatomical and histological studies of the metasternal and the Brindley's glands in the genus Triatoma are scarce and, considering the relevance of these exocrine glands, the present work aimed at studying their morphology in T. brasiliensis. The metasternal and the Brindley's glands of T. brasiliensis consist of glandular units similar to those described for Rhodnius prolixus Stål and Panstrongylus megistus Burmeister, comprising a secretory apparatus, saccule and collector duct.

Parasitoid increases survival of its pupae by inducing hosts to fight predators.

Many true parasites and parasitoids modify the behaviour of their host, and these changes are thought to be to the benefit of the parasites. However, field tests of this hypothesis are scarce, and it is often unclear whether the host or the parasite profits from the behavioural changes, or even if parasitism is a cause or consequence of the behaviour. We show that braconid parasitoids (Glyptapanteles sp.) induce their caterpillar host (Thyrinteina leucocerae) to behave as a bodyguard of the parasitoid pupae. After parasitoid larvae exit from the host to pupate, the host stops feeding, remains close to the pupae, knocks off predators with violent head-swings, and dies before reaching adulthood. Unparasitized caterpillars do not show these behaviours. In the field, the presence of bodyguard hosts resulted in a two-fold reduction in mortality of parasitoid pupae. Hence, the behaviour appears to be parasitoid-induced and confers benefits exclusively to the parasitoid.