Cesar Rodriguez-Saona

Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae)

Brown marmorated stink bug, Halyomorpha halys Stal, is an invasive, herbivorous insect species that was accidentally introduced to the United States from Asia. First discovered in Allentown, PA, in 1996, H. halys has now been reported from at least 40 states in the United States. Additional invasions have been detected in Canada, Switzerland, France, Germany, Italy, and Lichtenstein, suggesting this invasive species could emerge as a cosmopolitan pest species. In its native range, H. halys is classified as an outbreak pest; however, in North America, H. halys has become a major agricultural pest across a wide range of commodities. H. halys is a generalist herbivore, capable of consuming >100 different species of host plants, often resulting in substantial economic damage; its feeding damage resulted in US

Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid

37 million of losses in apple in 2010, but this stink bug species also attacks other fruit, vegetable, field crop, and ornamental plant species. H. halys has disrupted integrated pest management programs for multiple cropping systems. Pesticide applications, including broad-spectrum insecticides, have increased in response to H. halys infestations, potentially negatively influencing populations of beneficial arthropods and increasing secondary pest outbreaks. H. halys is also challenging because it affects homeowners as a nuisance pest; the bug tends to overwinter in homes and outbuildings. Although more research is required to better understand the ecology and biology of H. halys , we present its life history, host plant damage, and the management options available for this invasive pest species.

EXOGENOUS METHYL JASMONATE INDUCES VOLATILE EMISSIONS IN COTTON PLANTS

Herbivore-induced plants responses can affect the preference and performance of herbivores and their natural enemies. These responses may vary depending on the identity and number of herbivore species feeding on the plant so that when herbivores from different guilds feed on plants, the interactions between plants, herbivores, and natural enemies may be disrupted. Tomato plants were damaged either by the caterpillar Spodoptera exigua, or the aphid Macrosiphum euphorbiae, or damaged by both herbivores, or undamaged controls. We measured the preference and performance of S. exigua and its parasitoid Cotesia marginiventris, and activity of proteinase inhibitors (PI) as an indicator of induced resistance. Compared to undamaged plants, caterpillar damage reduced the number of eggs laid by S. exigua adults, reduced growth, consumption, and survival of larval S. exigua and C. marginiventris, and increased activity of PIs 43%; but did not increase attraction of C. marginiventris. While pupal mass of S. exigua was not affected, the pupal mass of C. marginiventris decreased on caterpillar-damaged plants compared to controls. In contrast, plants damaged by aphids were preferred for oviposition by S. exigua, and had increased larval consumption and survival, compared to controls. Aphid feeding did not affect the preference or performance of C. marginiventris, or PI activity, compared to controls. While oviposition was deterred on caterpillar-damaged plants, plants damaged by both herbivores received the same amount of oviposition as controls. The attraction of C. marginiventris to plants damaged by caterpillars and aphids was increased compared to controls. However, plants damaged by both herbivores had similar PI activity, larval growth and survival of S. exigua and C. marginiventris, as plants singly damaged by caterpillars. Overall, the preference component for both the herbivore and parasitoid was more strongly affected by damage due to multiple herbivores than the performance component.

Behavioral and electrophysiological responses of the emerald ash borer, Agrilus planipennis, to induced volatiles of Manchurian ash, Fraxinus mandshurica

We investigated the effect of exogenous methyl jasmonate (MeJA) on the emission of herbivore-induced volatiles; these volatile chemicals can signal natural enemies of the herbivore to the damaged plant. Exogenous treatment of cotton cv. Deltapine 5415 plants with MeJA induced the emission of the same volatile compounds as observed for herbivore-damaged plants. Cotton plants treated with MeJA emitted elevated levels of the terpenes (E)-β-ocimene, linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, (E,E)-α-farnesene, (E),-β-farnesene, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene compared to untreated controls. Other induced components included (Z)-3-hexenyl acetate, methyl salicylate, and indole. Methyl jasmonate treatment did not cause the release of any of the stored terpenes such as α-pinene, β-pinene, α-humulene, and (E)-β-caryophyllene. In contrast, these compounds were emitted in relatively large amounts from cotton due to physical disruption of glands by the herbivores. The timing of volatile release from plants treated with MeJA or herbivores followed a diurnal pattern, with maximal volatile release during the middle of the photoperiod. Similar to herbivore-treated plants, MeJA treatment led to the systemic induction of (Z)-3-hexenyl acetate, (E)-β-ocimene, linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, (E,E)-α-farnesene, (E)-β-farnesene, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene. Our results indicate that treatment of cotton with MeJA can directly and systemically induce the emission of volatiles that may serve as odor cues in the host-search behavior of natural enemies.

Herbivore-Induced Volatiles in the Perennial Shrub, Vaccinium corymbosum, and Their Role in Inter-branch Signaling

Summary.We investigated the volatile emissions of Manchurian ash seedlings, Fraxinus mandshurica, in response to feeding by the emerald ash borer, Agrilus planipennis, and to exogenous application of methyl jasmonate (MeJA). Feeding damage by adult A. planipennis and MeJA treatment increased volatile emissions compared to unexposed controls. Although the same compounds were emitted from plants damaged by beetles and treated with MeJA, quantitative differences were found in the amounts of emissions for individual compounds. Adult virgin female A. planipennis were similarly attracted to volatiles from plants damaged by beetles and those treated with MeJA in olfactometer bioassays; males did not respond significantly to the same volatiles. Coupled gas chromatographic-electroantennogram detection (GC-EAD) revealed at least 16 antennally-active compounds from F. mandshurica, including: hexanal, (E)-2-hexenal, (Z)-3-hexen-1-ol, 3-methyl-butylaldoxime, 2-methyl-butylaldoxime, (Z)-3-hexen-1-yl acetate, hexyl acetate, (E)-β-ocimene, linalool, 4,8-dimethyl-1,3,7-nonatriene, and E,E-α-farnesene. Electroantennogram (EAG) dose–response curves using synthetic compounds revealed that females had a stronger EAG response to linalool than males; and male responses were greater to: hexanal, (E)-2-hexenal, (Z)-3-hexen-1-ol, 3-methyl-butylaldoxime, 2-methyl-butylaldoxime, and hexyl acetate. These results suggest that females may use induced volatiles in long-range host finding, while their role for males is unclear. If attraction of females to these volatiles in an olfactometer is upheld by field experiments, host plant volatiles may find practical application in detection and monitoring of A. planipennis populations.

VOLATILE EMISSIONS TRIGGERED BY MULTIPLE HERBIVORE DAMAGE: BEET ARMYWORM AND WHITEFLY FEEDING ON COTTON PLANTS

Herbivore feeding activates plant defenses at the site of damage as well as systemically. Systemic defenses can be induced internally by signals transported via phloem or xylem, or externally transmitted by volatiles emitted from the damaged tissues. We investigated the role of herbivore-induced plant volatiles (HIPVs) in activating a defense response between branches in blueberry plants. Blueberries are perennial shrubs that grow by initiating adventitious shoots from a basal crown, which produce new lateral branches. This type of growth constrains vascular connections between shoots and branches within plants. While we found that leaves within a branch were highly connected, vascular connectivity was limited between branches within shoots and absent between branches from different shoots. Larval feeding by gypsy moth, exogenous methyl jasmonate, and mechanical damage differentially induced volatile emissions in blueberry plants, and there was a positive correlation between amount of insect damage and volatile emission rates. Herbivore damage did not affect systemic defense induction when we isolated systemic branches from external exposure to HIPVs. Thus, internal signals were not capable of triggering systemic defenses among branches. However, exposure of branches to HIPVs from an adjacent branch decreased larval consumption by 70% compared to those exposed to volatiles from undamaged branches. This reduction in leaf consumption did not result in decreased volatile emissions, indicating that leaves became more responsive to herbivory (or “primed”) after being exposed to HIPVs. Chemical profiles of leaves damaged by gypsy moth caterpillars, exposed to HIPVs, or non-damaged controls revealed that HIPV-exposed leaves had greater chemical similarities to damaged leaves than to control leaves. Insect-damaged leaves and young HIPV-exposed leaves had higher amounts of endogenous cis-jasmonic acid compared to undamaged and non-exposed leaves, respectively. Our results show that exposure to HIPVs triggered systemic induction of direct defenses against gypsy moth and primed volatile emissions, which can be an indirect defense. Blueberry plants appear to rely on HIPVs as external signals for inter-branch communication.

Molecular, Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

Plants are commonly attacked by more than one species of herbivore, potentially causing the induction of multiple, and possibly competing, plant defense systems. In the present paper, we determined the interaction between feeding by the phloem feeder silverleaf whitefly (SWF), Bemisia tabaci Gennadius (B-biotype = B. argentifolii Bellows and Perring), and the leaf-chewing beet armyworm (BAW), Spodoptera exigua Hübner, with regard to the induction of volatile compounds from cotton plants. Compared to undamaged control plants, infestation with SWF did not induce volatile emissions or affect the number and density of pigment glands that store volatile and nonvolatile terpenoid compounds, whereas infestation by BAW strongly induced plant volatile emission. When challenged by the two insect herbivores simultaneously, volatile emission was significantly less than for plants infested with only BAW. Our results suggest that tritrophic level interactions between cotton, BAW, and natural enemies of BAW, that are known to be mediated by plant volatile emissions, may be perturbed by simultaneous infestation by SWF. Possible mechanisms by which the presence of whiteflies may attenuate volatile emissions from caterpillar-damaged cotton plants are discussed.

Behavioral response of Lygus hesperus to conspecifics and headspace volatiles of alfalfa in a Y-tube olfactometer.

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and down-regulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dual-damaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.

A meta-analysis of insect pest behavioral manipulation with plant volatiles

The western tarnished plant bug, Lygus hesperus Knight, feeds and develops on a variety of weeds in the spring, with later generations moving to alfalfa and cotton where severe damage to reproductive structures can occur. A synthetic attractant for monitoring or mass-trapping L. hesperus, or the identification of potential attractants for natural enemies, would be useful tools for integrated pest management programs. Studies investigated the response of naive and experienced fifth-instar and adult L. hesperus to odors associated with conspecifics and alfalfa, Medicago sativa L. Fifth-instar L. hesperus responded to all plant/insect combinations, whereas female L. hesperus only responded preferentially to vegetative and flowering alfalfa where conspecifics had fed for 24–72 hr, and to vegetative alfalfa where conspecifics were added approximately 30 min before the test began. Males were not attracted to headspace volatiles from any of the alfalfa treatments. Analysis of headspace volatiles showed that (E)-2-hexanal, (Z)-3-hexen-1-ol, α-pinene, (Z)-3-hexenyl acetate, (E)-2-hexenyl acetate, limonene, (Z)-ocimene, (E)-β-ocimene, linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, and (E, E)-α-farnesene are emitted from both vegetative and flowering alfalfa. Indole and (3E, 7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene were only detected in flowering alfalfa. Damage to alfalfa by L. hesperus increased emissions of (Z)-ocimene, (E)-β-ocimene, (E)-β-caryophyllene, and (E, E)-α-farnesene, while β-pinene, myrcene, methyl salicylate, and (3E, 7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene were only detected from damaged plants. Thus, individual or mixtures of these alfalfa volatiles may be useful as attractants for capturing nymphs and adult females of L. hesperus in the field.

Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants.

Many insect pests utilize plant volatiles for host location and untangling the mechanisms of this process can provide tools for pest management. Numerous experimental results have been published on the effect of plant volatiles on insect pests. We used a meta‐analysis to summarize this knowledge and to look for patterns. Our goal was to identify herbivore and plant traits that might explain the herbivores’ behavioral response to plant volatiles in field applications. We scored a total of 374 unique plant volatile‐insect herbivore interactions obtained from 34 published studies investigating 50 herbivore pest species. Attractants had a significant effect on insect herbivore abundance but repellents did not; this latter result could be a result of the comparatively small number of field studies that tested plant volatiles as repellents (3%). Females were significantly more attracted to plant volatile baits than males. The diet breadth of herbivores was independent of a behavioral response to plant volatiles, but more case studies show effects of volatiles on chewers, followed by wood‐borers and sap‐feeders. There are more demonstrations of attraction to plant volatiles in Lepidoptera than in Thysanoptera. The method of plant volatile application had a significant effect on herbivore abundance and increasing the number of chemicals in individual baits attracted more herbivores. The magnitude of the response of herbivores to plant volatiles in forest and agricultural habitats was similar. We explore consistent patterns and highlight areas needing research in using plant volatiles to manage insect pests.