Podisus Maculiventris Research Articles

Do maternal allocations towards offspring quality and quantity ameliorate the effects of predators on offspring survival?

AbstractReproductive allocation is often balanced between the quantity and quality of offspring. Ecological stresses, like exposure to predators, can cause organisms to shift their allocations along this continuum. While the consequences of such plastic shifts for offspring performance are often untested, they are critical to understanding the potential long‐term benefits of manipulating predation risk as an agricultural pest management technique. Predation risk induces reductions in egg production and increases in nutritional condition due to maternal provisioning in Colorado potato beetles (Leptinotarsa decemlineata, CPB). Here, we tested whether reductions in density or increases in offspring condition, which may increase per‐capita larval survival, can compensate for the reduction in total egg production, especially when offspring are exposed to predators. In two field trials, we manipulated density and condition of larval CPB and measured survival through development to adulthood in field cages with and without predaceous stink bugs (Podisus maculiventris). As expected, cages with the higher initial larval densities had more larvae and adults surviving in the treatments without predators – about 30%–50% survival across densities. When predators were present, this relationship did not hold because of density‐dependent predation. Larval condition interacted with density and impacted larval survival in both trials albeit in different ways. In trial 1, unprovisioned beetles had higher survival at the higher densities; in trial 2, provisioned beetles had higher survival across densities. Synthesis and Applications: Overall, our test of the effects of predation risk via manipulations of larval density and condition revealed few net compensatory benefits to the prey of reduced density and higher condition. Benefits to the prey of shifts in allocation from the quantity to quality of offspring may depend on factors that influence the strength of density dependence, including predation intensity. Our results suggest a new strategy of taking advantage of the reductions in prey density due to non‐consumptive effects of predators as a pest management approach to protect plants.

Exploring the anti-biofilm activity and Suppression of virulence genes expression by thanatin in Listeria monocytogenes

Listeria monocytogenes is a common foodborne pathogen causing severe listeriosis, with a mortality rate of 20–30%. This pathogen spreads through biofilm formation in the food industry. Antimicrobial peptides are widely used in food preservation to combat harmful pathogens. Thanatin, a 21-amino acid peptide from Podisus maculiventris, combats various pathogens effectively. This study aimed to evaluate the antimicrobial efficacy of thanatin peptide against L. monocytogenes ATCC 19115. The minimum inhibitory concentration (MIC) of thanatin against L. monocytogenes was determined to be 17 μg/mL. Analysis using a scanning electron microscope (SEM) confirmed its antibacterial efficacy. Thanatin treatment inhibited swimming motility, biofilm formation, auto-aggregation, cytotoxicity, hemolysin activity, adhesion, and host cell invasion by L. monocytogenes. Concentrations ranging from 1/16MIC (27%) to MIC (92%) effectively prevented biofilm formation, and existing biofilms experienced significant reduction (9.41%–80.66%) after thanatin treatment. Moreover, the thanatin peptide exhibited significant cytotoxic effects on Caco-2 cancer cells (IC50 = 27.04 μg/mL) and decreased the hemolytic activity of L. monocytogenes (2.66%–7.33%). Additionally, thanatin effectively suppressed the expression of virulence genes in L. monocytogenes, decreasing its pathogenicity. In summary, thanatin peptide exhibits beneficial antibacterial effects, suggesting its potential as a natural bacteriostatic agent for further research and practical implementation.

Predator densities alter the influence of non‐consumptive effects on the population dynamics of an agricultural pest

Abstract Augmentative release of predators is used in agriculture to suppress pest populations and minimise crop damage. However, predators affect prey populations not only through consumption but by inducing changes to prey morphology, physiology, behaviour and life history. These risk‐induced trait responses can increase prey fitness, potentially reducing the efficacy of certain predators as biocontrol agents. We investigated how non‐consumptive effects contribute to the overall influence of predators by modelling the effect of the predator Podisus maculiventris on the population dynamics of a major agricultural pest, the Colorado potato beetle (Leptinotarsa decemlineata). We developed a demographic model incorporating both consumption and non‐consumptive Podisus‐induced shifts in beetle reproductive strategy. Our model combines data from multiple mechanistic experiments showing that predator‐exposed beetles produce fewer offspring but increase offspring provisioning, and that provisioned larvae have increased survival when predators are present. We simulated beetle densities across multiple beetle generations and a range of predator densities. The influence of non‐consumptive effects depended on predator density. At low predator densities, non‐consumptive effects strengthened the negative effect of predators by up to 45%, and risk‐induced changes to offspring provisioning had a stronger effect on prey densities than reduced offspring quantity. In contrast, at high predator densities, non‐consumptive effects changed the effect of predators by <5%, likely because beetle densities were very low both with and without non‐consumptive effects. Our results suggest that even adaptive responses to predation risk by prey do not necessarily reduce the ability of predators to suppress pest populations.

Field releases of the exotic parasitoid Trissolcus japonicus (Hymenoptera: Scelionidae) and survey of native parasitoids attacking Halyomorpha halys (Hemiptera: Pentatomidae) in Michigan.

An adventive population of the exotic parasitoid wasp, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), discovered in Michigan in 2018, is a promising biological control agent of the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Following its discovery, field releases of Tr. japonicus were conducted over 2 yr in southern Michigan, to test how release size or release frequency impacts establishment. Sentinel eggs of H. halys and of the native Podisus maculiventris (Say) (Hemiptera: Pentatomidae) were used alongside yellow sticky cards to monitor parasitoids. In 2019 and 2020, 7,200 Tr. japonicus were released at 16 sites. Monitoring between 2019 and 2021 yielded only 49 individuals. The captures suggest reproductive activity and overwintering success in the field but do not allow for evaluation of best release methods. Parasitism by native parasitoids was below 7%, which is similar to other states and unlikely to provide sufficient control of H. halys. The placement of sentinel eggs or sticky traps either in the lower or middle canopy of trees did not influence parasitoid capture rates. Frozen and fresh H. halys sentinel eggs were attacked at the same rate, but more native parasitoids emerged from frozen eggs. We did not find signs of nontarget effects on P. maculiventris thus parasitism rates overall were very low. These results could indicate dispersal of Tr. japonicus from the release sites or slow population growth. The latter may be due to the relatively low densities of H. halys in Michigan or may stem from the small founding size of our laboratory colony.

Discovery, characterization, and redesign of potent antimicrobial thanatin orthologs from Chinavia ubica and Murgantia histrionica targeting E. coli LptA

Podisus maculiventris thanatin has been reported as a potent antimicrobial peptide with antibacterial and antifungal activity. Its antibiotic activity has been most thoroughly characterized against E. coli and shown to interfere with multiple pathways, such as the lipopolysaccharide transport (LPT) pathway comprised of seven different Lpt proteins. Thanatin binds to E. coli LptA and LptD, thus disrupting the LPT complex formation and inhibiting cell wall synthesis and microbial growth. Here, we performed a genomic database search to uncover novel thanatin orthologs, characterized their binding to E. coli LptA using bio-layer interferometry, and assessed their antimicrobial activity against E. coli. We found that thanatins from Chinavia ubica and Murgantia histrionica bound tighter (by 3.6- and 2.2-fold respectively) to LptA and exhibited more potent antibiotic activity (by 2.1- and 2.8-fold respectively) than the canonical thanatin from P. maculiventris. We crystallized and determined the LptA-bound complex structures of thanatins from C. ubica (1.90 Å resolution), M. histrionica (1.80 Å resolution), and P. maculiventris (2.43 Å resolution) to better understand their mechanism of action. Our structural analysis revealed that residues A10 and I21 in C. ubica and M. histrionica thanatin are important for improving the binding interface with LptA, thus overall improving the potency of thanatin against E. coli. We also designed a stapled variant of thanatin that removes the need for a disulfide bond but retains the ability to bind LptA and antibiotic activity. Our discovery presents a library of novel thanatin sequences to serve as starting scaffolds for designing more potent antimicrobial therapeutics.

Semiochemical Release and Ontogenetic Changes in a Primary Scent Gland of Podisus maculiventris.

The spined shoulder bug, Podisus maculiventris, is a generalist predator studied for its biocontrol potential. Despite our growing understanding of gland development, the conditions that elicit releases are largely unknown. To determine if male age or gland development affects the chemical composition and release behavior, we dissected adult male bugs and profiled the chemical composition of the male DAG 1, 7, and 14 d post-eclosion. To determine if gland development is related to sexual maturity, we counted the number of sperm present in the seminal vesicles at the same time points. Finally, we measured the diurnal release patterns of different aged males and in various male-female combinations. We observed that newly eclosed adults have under-developed glands and male seminal vesicles contained few sperm. One week post-eclosion the DAG contained previously reported semiochemical compounds and males contained many sperm. Mirroring the trend in reproductive maturation and gland development, the number of semiochemical releases increased with age and the majority of releases followed a scotophase pattern unaffected by sexual composition. These findings link male age to 1) dorsal abdominal gland development 2) release behavior and 3) sexual maturity, which will help our understanding of when these olfactory cues are present for other organisms, like prey, to perceive. Given the results, releasing adults that are at least 1week post eclosion will maximize the non-consumptive effects of this biocontrol agent.

Non-target attack of the native stink bug, Podisus maculiventris by Trissolcus japonicus, comes with fitness costs and trade-offs

Accidentally introduced parasitoids can provide biological control of the invasive pest they followed but could also pose a threat to native species if they are not specialists. Attack of native species could reduce the effectiveness of adventive natural enemies if it is accompanied by reduced fitness, and it may increase acceptance of non-target species. We tested how intermittent host shift and prolonged exposure to a non-target, native species Podisus maculiventris (Say) (Hemiptera: Pentatomidae) may affect the fitness and host acceptance of the egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) that was co-introduced with the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In the first experiment, replicate parasitoid populations were reared either with or without a history of host switching over a 10-generation period between the native and the invasive stink bug that was followed by three generations of continuous reproduction on either host. In the second experiment, replicated populations were exposed for three continuous generations to either the native or invasive host. Occasional or prolonged reproduction on the native host did not increase acceptance and developmental success on the non-target species. Emergence rate of T. japonicus was consistently lower when it reproduced on the native stink bug. There was also a trade-off for the parasitoid, in terms of reduced emergence rate, when switching back to H. halys from the native host. These results suggest that host shifts to native species could reduce the effectiveness of T. japonicus at attacking H. halys, but the fitness costs may prevent significant non-target effects in nature.

Low water availability enhances volatile‐mediated direct defences but disturbs indirect defences against herbivores

Abstract Interactions between plants and natural enemies of insect herbivores influence plant productivity and survival by reducing herbivory. Plants attract natural enemies via herbivore‐induced plant volatiles (HIPVs), but how water availability (WA) influences HIPV‐mediated defences is unclear. We use tomato, Solanum lycopersicum, tomato fruitworm, Helicoverpa zea and two natural enemies, the parasitoid wasp, Microplitis croceipes and the predator spined soldier bug, Podisus maculiventris, to investigate the effect of WA on HIPV emission dynamics and associated plant defence. We show that low WA initially increases total HIPV emission by tomato on the first day of herbivore exposure and, in contrast, reduces HIPV emission on the second day. Low WA enhances HIPVs that are mostly found in tomato trichomes. Notably, some volatiles inhibited by low WA are known attractants of natural enemies. Evidence from Y‐tube and in‐cage behavioural assays indicates that changes in HIPV emissions by low WA compromise the ability of tomato plants to attract natural enemies. Synthesis. Based on our results, we propose a hypothesis where plants respond to low WA by enhancing repellent HIPV emissions and reducing the emission of HIPVs that attract natural enemies, which disrupts natural enemy‐mediated plant indirect defences, but enhances plant direct defence against herbivores.

The threat of parasitism impairs immune function in host caterpillars

AbstractNonconsumptive effects (NCE) from natural enemy presence are known to change the behavior, morphology, and development of potential victims. However, the overwhelming majority of these studies focus on predation, documenting changes in prey behavior; far less is understood about parasitism risk and impacts on host physiology. We used the caterpillar Manduca sexta (Lepidoptera: Sphingidae) and two of its main natural enemies—a specialist parasitoid (wasp), Cotesia congregata (Hymenoptera: Braconidae), and a generalist predator (soldier bug), Podisus maculiventris (Hemiptera: Pentatomidae)—to determine how the threat of parasitism and predation during larval development alter prey growth and immunity. Caterpillars developing near female predators and parasitoids were ~ 85% larger compared to individuals without enemy exposure. Development time was not affected by natural enemies when compared to controls, but male P. maculiventris slowed M. sexta development compared to the other natural enemies. For immune functionality, phenoloxidase (PO) activity only responded to parasitoids, with wasp‐exposed caterpillars exhibiting 35% lower PO activity than all other treatments, while lysozyme activity was unaffected by any enemy treatment. This work emphasizes that parasites can induce changes to host immunity that potentially affect wasp development. More broadly, NCEs on victim immunity are likely given immunity's contribution to host defense but have been under‐appreciated compared to more easily observed phenotypes like behavior and morphology.

Negative Effects of Rhizobacteria Association on Plant Recruitment of Generalist Predators.

Plant-associated microbes can influence above- and belowground interactions between plants and other organisms and thus have significant potential for use in the management of agricultural ecosystems. However, fully realizing this potential will require improved understanding of the specific ways in which microbes influence plant ecology, which are both more complex and less well studied than the direct effects of microbes on host-plant physiology. Microbial effects on mutualistic and antagonistic interactions between plants and insects are of particular interest in this regard. This study examines the effects of two strains of Pseudomonas rhizobacteria on the direct and indirect (predator-mediated) resistance of tomato plants to a generalist herbivore (Spodoptera littoralis) and associated changes in levels of defense compounds. We observed no significant effects of rhizobacteria inoculation on caterpillar weight, suggesting that rhizobacteria did not influence direct resistance. However, the generalist predator Podisus maculiventris avoided plants inoculated with one of our rhizobacteria strains, Pseudomonas simiae. Consistent with these results, we found that inoculation with P. simiae influenced plant volatile emissions, but not levels of defense-related compounds. These findings show that rhizobacteria can negatively affect the attraction of generalist predators, while highlighting the complexity and context dependence of microbial effects on plant–insect interactions.

Choice behavior of the generalist pentatomid predator Podisus maculiventris when offered lepidopteran larvae infected with an entomopathogenic fungus

Choice behavior of the generalist pentatomid predator Podisus maculiventris when offered lepidopteran larvae infected with an entomopathogenic fungus

Масс-спектрометрические исследования состава газовыделения живых организмов

The quantitative and qualitative composition of volatile organic compounds (VOCs) of human exhaled air, the air environment of various types of entomopathogenic fungi (EPF) of the genus Lecanicillium, used as an alternative to chemical pesticides to protect plants from pests, cabbage moth caterpillars, as well as spined soldier bug from the shield family, was studied using a quadrupole mass spectrometer. The main components found were acetone, acetic acid, and isoprene. These components in human exhalation are significant indicators for non-invasive disease diagnosis. For the first time, sulfur dioxide was found in the composition of VOC EPF, as one of the possible repellents. The caterpillars of cabbage moth secrete exclusively acetic acid.

Mass spectrometric gas release composition studies of living organisms

The quantitative and qualitative composition of volatile organic compounds (VOCs) of human exhaled air, the air environment of various types of entomopathogenic fungi (EPF) of the genus Lecanicillium, used as an alternative to chemical pesticides to protect plants from pests, cabbage moth caterpillars, as well as spined soldier bug from the shield family, was studied using a quadrupole mass spectrometer. The main components found were acetone, acetic acid, and isoprene. These components in human exhalation are significant indicators for non-invasive disease diagnosis. For the first time, sulfur dioxide was found in the composition of VOC EPF, as one of the possible repellents. The caterpillars of cabbage moth secrete exclusively acetic acid. Keywords: mass spectrometry, volatile organic compounds analysis, exhaled air, entomopathogenic fungi, Mamestra brassicae L., Podisus maculiventris S.

Non-Target Attack of the Native Stink Bug, Podisus Maculiventris by Trissolcus Japonicus, Comes with Fitness Costs and Trade-Offs

Non-Target Attack of the Native Stink Bug, Podisus Maculiventris by Trissolcus Japonicus, Comes with Fitness Costs and Trade-Offs

Ecological impacts of the invasive plant Xanthium strumarium and the impacts of three aboveground herbivores on the invader

Exotic plant invasions are generally assumed to negatively impact biodiversity of recipient communities. However, experimental evidence for this assumption is little, especially in developing countries. In addition, there is hardly applicable method to control invasive plants. Enemy release is often hypothesized to facilitate exotic plant invasions, thus re-association with natural enemies of invasive ranges may inhibit invasions of exotic plants, and these enemies may have the potential to be used as biological control agents for these invaders. To address above problems, we determined abundance of the invasive plant Xanthium strumarium, its impacts on co-occurring native plants, and abundances of three herbivores and their impacts on the invader at five sites in the rice tract of Punjab, Pakistan. Relative abundance of the invader varied greatly among the study sites, ranging from 3.5% to 50.4%. The invader significantly reduced abundance of co-occurring native plants at all study sites, and their richness and evenness at some sites with high abundances of the invader. The polyphagous insects Phenacoccus solenopsis, Podisus maculiventris and Spodoptera frugiperda were all found on the invader (not on crops) at all study sites, which significantly reduced growth of the invader. The abundance of P. solenopsis on the invader was much higher than those of P. maculiventris and S. frugiperda. The abundances of the herbivores were significantly higher at sites with high relative to low relative abundances of the invader. Our study indicates that natural enemies may accumulate on invasive plants with the increase of their abundance and/or invasion time, inhibiting further invasions, and provides evidence for enemy release hypothesis. More studies are needed to determine whether these herbivores, especially P. solenopsis, could be used as biological control agents for the invader.

Trissolcus japonicus foraging behavior: Implications for host preference and classical biological control

The brown marmorated stink bug, Halyomorpha halys, is an alien pest native to East Asia, which in the past two decades has invaded USA, Europe and other countries around the globe, causing severe economic losses and public nuisance. The Asian egg parasitoid Trissolcus japonicus is the most promising agent currently under study for the classical biological control of H. halys. The foraging behavior of this wasp was investigated in response to chemical traces – ‘footprints’ – deposited by its host H. halys and by a suboptimal predatory host species, the spined soldier bug, Podisus maculiventris. Motion tracking software (Ethovision) was employed to record and analyze the behavior of T. japonicus on stink bug-contaminated and on control substrates. Wasps exhibited a ‘motivated searching’ behavior (i.e. longer residence time, slower walking velocity, higher angular velocity and coverage of greater distances) in response to footprints originating from females and from males of both species compared to blank controls. However, this searching behavior was significantly more intense on H. halys footprints, compared to those of P. maculiventris. Moreover, T. japonicus significantly intensified its searching on footprints of all mobile nymphal instars of H. halys, but not on those of P. maculiventris nymphs. Additionally, the longevity of H. halys female trails was assessed, and footprints remained bioactive, eliciting a consistent searching behavior in the wasp for 72 h after initial deposition. A series of GC–MS chemical analyses revealed components of these trails, with n-tridecane and (E)-2-decenal found to be the most abundant, and probably the key components of the kairomone utilized by the wasp for short range host location. Solutions of the synthetic compounds were tested both together and singly. The blend of n-tridecane and (E)-2-decenal (4: 1) significantly prolonged the residence time of T. japonicus, as did n-tridecane alone. These results are discussed in the context of host preference and classical biological control.

Photoprotective egg pigmentation reduces negative carryover effects of ultraviolet radiation on stink bug nymph survival

Solar ultraviolet radiation (UV) can have a wide range of negative effects on animal fitness that take place not only during, but also after exposure (carryover effects). UV-induced carryover effects and potential adaptations to avoid or mitigate them are understudied in terrestrial animals, including arthropods and their potentially most vulnerable life stages. The spined soldier bug, Podisus maculiventris, increases the emergence of its eggs that are exposed to UV radiation by coating them in sunscreen-like pigmentation, but consequences of these conditions of embryonic development for nymphs and adults are unknown. We measured stink bug nymph survival, adult size and sex ratio following exposure of differently pigmented eggs across a range of UV intensities. Nymph survival to adulthood decreased with higher intensity of embryonic UV exposure and this carryover effect decreased with higher level of egg pigmentation, similar to previously observed effects on embryonic survival. Nymph development time, adult size and sex ratio were not affected by embryonic exposure to UV radiation nor by photoprotective egg pigmentation. This study is the first to demonstrate the potential for lethal carryover effects of UV radiation in terrestrial insects, highlighting the need for more studies of how this pervasive environmental stressor can affect fitness across life stages.

Neonicotinoid Exposures that Stimulate Predatory Stink Bug, Podisus maculiventris (Hemiptera: Pentatomidae), Reproduction Do Not Inhibit Its Behavior.

Exposure to sublethal amounts of pesticide can compromise life-history traits and behavior of natural enemies thereby reducing their effectiveness as predators. However, sublethal exposures to pesticides and other stressors may also stimulate insects, a dose-response phenomenon known as hormesis. We previously reported stimulatory effects on reproduction in the beneficial insect predator Podisus maculiventris (Say) (Hemiptera: Pentatomidae) following exposure to sublethal concentrations of imidacloprid. Here we examined whether these same treatments stimulated behavior and/or predation of P. maculiventris. Stimulation of some behaviors occurred at a reproductively hormetic concentration and two additional sublethal concentrations, depending upon bioassay design and sex. We observed no substantial inhibition of behavior or predation at a reproductively hormetic concentration, demonstrating that reproductive fitness in P. maculiventris may be stimulated without compromising behaviors important in its effectiveness as a natural enemy.

Learning can be detrimental for a parasitic wasp.

Animals have evolved the capacity to learn, and the conventional view is that learning allows individuals to improve foraging decisions. The parasitoid Telenomus podisi has been shown to parasitize eggs of the exotic stink bug Halyomorpha halys at the same rate as eggs of its coevolved host, Podisus maculiventris, but the parasitoid cannot complete its development in the exotic species. We hypothesized that T. podisi learns to exploit cues from this non-coevolved species, thereby increasing unsuccessful parasitism rates. We conducted bioassays to compare the responses of naïve vs. experienced parasitoids on chemical footprints left by one of the two host species. Both naïve and experienced females showed a higher response to footprints of P. maculiventris than of H. halys. Furthermore, parasitoids that gained an experience on H. halys significantly increased their residence time within the arena and the frequency of re-encounter with the area contaminated by chemical cues. Hence, our study describes detrimental learning where a parasitoid learns to associate chemical cues from an unsuitable host, potentially re-enforcing a reproductive cul-de-sac (evolutionary trap). Maladaptive learning in the T. podisi—H. halys association could have consequences for population dynamics of sympatric native and exotic host species.

Thanatin: An Emerging Host Defense Antimicrobial Peptide with Multiple Modes of Action.

Antimicrobial peptides (AMPs) possess great potential for combating drug-resistant bacteria. Thanatin is a pathogen-inducible single-disulfide-bond-containing β-hairpin AMP which was first isolated from the insect Podisus maculiventris. The 21-residue-long thanatin displays broad-spectrum activity against both Gram-negative and Gram-positive bacteria as well as against various species of fungi. Remarkably, thanatin was found to be highly potent in inhibiting the growth of bacteria and fungi at considerably low concentrations. Although thanatin was isolated around 25 years ago, only recently has there been a pronounced interest in understanding its mode of action and activity against drug-resistant bacteria. In this review, multiple modes of action of thanatin in killing bacteria and in vivo activity, therapeutic potential are discussed. This promising AMP requires further research for the development of novel molecules for the treatment of infections caused by drug resistant pathogens.