Yigen Chen

Effects of nitrogen fertilization on tritrophic interactions

Tritrophic interactions (plant—herbivore—natural enemy) are basic components of nearly all ecosystems, and are often heavily shaped by bottom-up forces. Numerous factors influence plants’ growth, defense, reproduction, and survival. One critical factor in plant life histories and subsequent trophic levels is nitrogen (N). Because of its importance to plant productivity, N is one of the most frequently used anthropogenic fertilizers in agricultural production and can exert a variety of bottom-up effects and potentially significantly alter tritrophic interactions through various mechanisms. In this paper, the potential effects of N on tritrophic interactions are reviewed. First, in plant-herbivore interactions, N availability can alter quality of the plant (from the herbivore’s nutritional perspective) as food by various means. Second, nitrogen effects can extend directly to natural enemies through herbivores by changes in herbivore quality vis-à-vis the natural enemy, and may even provide herbivores with a defense against natural enemies. Nitrogen also may affect the plant’s indirect defenses, namely the efficacy of natural enemies that kill herbivores attacking the plant. The effects may be expressed via (1) quantitatively and/or qualitatively changing herbivore-induced plant volatiles or other plant features that are crucial for foraging and attack success of natural enemies, (2) modifying plant architecture that might affect natural enemy function, and (3) altering the quality of plant-associated food and shelter for natural enemies. These effects, and their interactive top–down and bottom-up influences, have received limited attention to date, but are of growing significance with the need for expanding global food production (with accompanying use of fertilizer amendments), the widening risks of fertilizer pollution, and the continued increase in atmospheric CO2.

Physiological, nutritional, and biochemical bases of corn resistance to foliage-feeding fall armyworm.

Three corn (Zea mays) germplasm lines [i.e., Ab24E (susceptible control), Mp708 (resistant control), and a locally selected partial inbred line FAW7050 (resistant)] were examined for Spodoptera frugiperda (J.E. Smith; Lepidoptera: Noctuidae) resistance. Nutritional [i.e., total protein content, amino acids, glucose, total nonstructural carbohydrates (TNC), protein to TNC (P/C) ratios] and biochemical (i.e., peroxidase and lipoxygenase 3) properties in the seedlings of these corn lines were examined to categorize resistance mechanisms to S. frugiperda. Physiological changes in photosynthetic rates also were examined in an attempt to explain nutritional and biochemical dynamics among corn germplasm lines and between insect-infested and noninfested corn plants within a germplasm line. Results indicated that S. frugiperda larvae survived better and developed faster in susceptible Ab24E than in resistant FAW7050 or Mp708. The three germplasm lines differed in resistance mechanisms to S. frugiperda, and the observed patterns of resistance were probably collective results of the P/C ratio and defensive proteins. That is, the susceptibility of Ab24E to S. frugiperda was due to a high P/C ratio and a low level of induced defensive compounds in response to insect herbivory, while the resistance of FAW7050 resulted from elevated defensive proteins following insect herbivory, low P/C ratio, and elevated defensive proteins in Mp708 contributed to its resistance to S. frugiperda. The elevated protein amounts in resistant Mp708 and FAW7050 following S. frugiperda injury were likely due to greater conversion of photosynthates to defensive proteins following the greater photosynthetic rates in these entries. Greater photosynthetic capacity in Mp708 and FAW7050 also led to higher amino acid and glucose contents in these two lines. Neither amino acid nor lipoxygenase 3 played a critical role in corn resistance to S. frugiperda. However, high inducibility of peroxidase may be an indicator of S. frugiperda susceptibility as observed elsewhere.

Role of Emerald Ash Borer (Coleoptera: Buprestidae) Larval Vibrations in Host-Quality Assessment by Tetrastichus planipennisi (Hymenoptera: Eulophidae)

ABSTRACT The biological control agent Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) is a gregarious larval endoparasitoid of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), an invasive cambium-feeding species responsible for recent, widespread mortality of ash (Fraxinus spp.) in North America. T. planipennisi is known to prefer late-instar emerald ash borer, but the cues used to assess host size by this species and most other parasitoids of concealed hosts remain unknown. We sought to test whether vibrations produced by feeding emerald ash borer vary with larval size and whether there are any correlations between these cues and T. planipennisi progeny number (i.e., brood size) and sex ratio. The amplitudes and rates of 3–30-ms vibrational impulses produced by emerald ash borer larvae of various sizes were measured in the laboratory before presenting the larvae to T. planipennisi. Impulse-rate did not vary with emerald ash borer size, but vibration amplitude was significantly higher for large larvae than for small larvae. T. planipennisi produced a significantly higher proportion of female offspring from large hosts than small hosts and was shown in previous work to produce more offspring overall from large hosts. There were no significant correlations, however, between the T. planipennisi progeny data and the emerald ash borer sound data. Because vibration amplitude varied significantly with host size, however, we are unable to entirely reject the hypothesis that T. planipennisi and possibly other parasitoids of concealed hosts use vibrational cues to assess host quality, particularly given the low explanatory potential of other external cues. Internal chemical cues also may be important.

Interactive Influence of Leaf Age, Light Intensity, and Girdling on Green Ash Foliar Chemistry and Emerald Ash Borer Development

Biotic and abiotic environmental factors affect plant nutritional quality and defensive compounds that confer plant resistance to herbivory. Influence of leaf age, light availability, and girdling on foliar nutrition and defense of green ash (Fraxinus pennsylvanica Marsh) was examined in this study. Longevity of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), adults reared on green ash foliage subjected to these factors was assayed. Mature leaves generally were more nutritious with greater amino acids and a greater ratio of protein to non-structural carbohydrate (P:C) than young leaves, in particular when trees were grown in shade. On the other hand, mature leaves had lower amounts of trypsin and chymotrypsin inhibitors, and total phenolics compared to young leaves. Lower defense of mature leaves alone, or along with higher nutritional quality may lead to increased survival and longevity of emerald ash borer feeding on mature leaves. Sunlight reduced amino acids and P:C ratio, irrespective of leaf age and girdling, and elevated total protein of young foliage, but not protein of mature leaves. Sunlight also dramatically increased all investigated defensive compounds of young, but not mature leaves. Girdling reduced green ash foliar nutrition, especially, of young leaves grown in shade and of mature leaves grown in sun. However emerald ash borer performance did not differ when fed leaves from trees grown in sun or shade, or from girdled or control trees. One explanation is that emerald ash borer reared on lower nutritional quality food may compensate for nutrient deficiency by increasing its consumption rate. The strong interactions among leaf age, light intensity, and girdling on nutrition and defense highlight the need for caution when interpreting data without considering possible interactions.

Moisture content and nutrition as selection forces for emerald ash borer larval feeding behaviour

1. The exotic phloem‐feeding emerald ash borer (EAB), Agrilus planipennis, has killed tens of millions of North American ash trees (Fraxinus) since its first detection in the U.S.A. in 2002. Ash trees are killed by larval feeding in the cambial region, which disrupts translocation of photosynthates and nutrients.

Differential Response in Foliar Chemistry of Three Ash Species to Emerald Ash Borer Adult Feeding

The emerald ash borer (EAB; Agrilus planipennis Fairmaire; Coleoptera: Buprestidae), is an exotic wood-boring beetle that has been threatening North American ash (Fraxinus spp.) resources since its discovery in Michigan and Ontario in 2002. In this study, we investigated the phytochemical responses of the three most common North American ash species (black, green, and white ash) in northeastern USA to EAB adult feeding. Black ash was the least responsive to EAB adult feeding in terms of the induction of volatile compounds, and levels of only two (indole and benzyl cyanide) of the 11 compounds studied increased. In green ash, levels of two [(E)-β-ocimene and indole] of the 11 volatile compounds studied were elevated, while the levels of two green leaf volatiles [hexanal and (E)-2-hexenal] decreased. White ash showed the greatest response with an increase in levels of seven of the 11 compounds studied. Qualitative differences among ash species were detected. Among the phenolic compounds detected, ligustroside was the only one detected in all three species. Oleuropein aglycone and 2 unidentified compounds were found only in black ash; coumaroylquinic acid and feruloylquinic acid were detected only in green ash; and verbascoside hexoside was detected only in white ash. EAB adult feeding did not elicit or decrease concentrations of any selected individual phenolic compounds. However, although levels of total phenolics from black and green ash foliage were not affected by EAB adult feeding, they decreased significantly in white ash. EAB adult feeding elevated chymotrypsin inhibitors in black ash. The possible ecological implications of these findings are discussed.

Feeding by emerald ash borer larvae induces systemic changes in black ash foliar chemistry.

The exotic wood-boring pest, emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), has been threatening North American ash (Fraxinus spp.) resources, this being recognized since its first detection in Michigan, USA and Ontario, Canada in 2002. Ash trees are killed by larval feeding in the cambial region, which results in disruption of photosynthate and nutrient translocation. In this study, changes in volatile and non-volatile foliar phytochemicals of potted 2-yr-old black ash, Fraxinus nigra Marshall, seedlings were observed in response to EAB larval feeding in the main stem. EAB larval feeding affected levels of six compounds [hexanal, (E)-2-hexenal, (Z)-3-hexenyl acetate, (E)-β-ocimene, methyl salicylate, and (Z,E)-α-farnesene] with patterns of interaction depending upon compounds of interest and time of observation. Increased methyl salicylate emission suggests similarity in responses induced by EAB larval feeding and other phloem-feeding herbivores. Overall, EAB larval feeding suppressed (Z)-3-hexenyl acetate emission, elevated (E)-β-ocimene emission in the first 30days, but emissions leveled off thereafter, and generally increased the emission of (Z,E)-α-farnesene. Levels of carbohydrates and phenolics increased overall, while levels of proteins and most amino acids decreased in response to larval feeding. Twenty-three amino acids were consistently detected in the foliage of black ash. The three most abundant amino acids were aspartic acid, glutamic acid, glutamine, while the four least abundant were α-aminobutyric acid, β-aminoisobutyric acid, methionine, and sarcosine. Most (16) foliar free amino acids and 6 of the 9 detected essential amino acids decreased with EAB larval feeding. The ecological consequences of these dynamic phytochemical changes on herbivores harbored by ash trees and potential natural enemies of these herbivores are discussed.

Differential utilization of ash phloem by emerald ash borer larvae: Ash species and larval stage effects

1 Two experiments were performed to determine the extent to which ash species (black, green and white) and larval developmental stage (second, third and fourth instar) affect the efficiency of phloem amino acid utilization by emerald ash borer (EAB) Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) larvae. 2 EAB larvae generally utilized green ash amino acids more efficiently than those of the other two species. For example, the concentrations of only six (two essential) and seven (two essential) amino acids were lower in frass from EAB that fed upon black and white ash than in the corresponding phloem, respectively. By contrast, concentrations of 16 (eight essential) amino acids were lower in the frass from EAB that fed upon green ash than in the phloem. In addition, in green ash, the frass : phloem ratios of 13 amino acids were lower than their counterparts in black and white ash. 3 The concentrations of non‐essential amino acids glycine and hydroxylproline were greater in frass than in phloem when EAB fed on black ash, although not when EAB fed on green or white ash. 4 The concentration of total phenolics (a group of putative defensive compounds to EAB, expressed as antioxidant activity of acetone extraction) was high in EAB frass but even higher in the phloem samples when the data were pooled across ash species and EAB larval stages. This suggests EAB larvae may eliminate phenolics through a combination of direct excretion and enzymatic conversion of phenolics to nonphenolics before excretion. Because the ratio of frass total phenolics to phloem total phenolics in white ash was lower than the ratios in black and green ash, the ability to destroy phenolics or convert them to nonphenolics was greater when EAB larvae fed on white ash. 5 Fourth‐instar EAB extracted phloem amino acids, including threonine, more efficiently than third‐instar EAB. The different larval developmental stages of EAB did not differ in their apparent ability to destroy phenolics or convert them to nonphenolics.

Changes of Oxidase and Hydrolase Activities in Pecan Leaves Elicited by Black Pecan Aphid (Hemiptera: Aphididae) Feeding

ABSTRACT The black pecan aphid, Melanocallis caryaefoliae (Davis) (Hemiptera: Aphididae), is a foliar feeder of pecan, Carya illinoinensis (Wangenh.) K. Koch (Juglandaceae). The pest causes chlorosis of leaflet lamina, physiological damage to foliage and trees, and commonly limits the profitability of commercial pecan orchard enterprises. However, key aspects of this host-pest interaction are poorly understood. We report here the effects of M. caryaefoliae feeding on the foliar activity of oxidative (i.e., catalase, lipoxygenase [LOX]-1 and 3, and peroxidase) andhydrolytic (i.e., esterase) enzymes in relation to the degree of aphid resistance among pecan varieties. The 2-yr study showed that M. caryaefoliae-infested foliage exhibited elevated peroxidase activity only in susceptible (‘Desirable’, ‘Sumner’, and ‘Schley’), but not in resistant (‘Cape Fear’, ‘Gloria Grande’, and ‘Money Maker’) genotypes. Susceptible genotypes also exhibited more severe leaf chlorosis in response to M. caryaefoliae feeding than the resistant genotypes; however, the aphid feeding did not influence catalase or esterase activity in all varieties, except the increase of esterase activity in Desirable and Gloria Grande. Melanocallis caryaefoliae feeding also influences activity of two lipoxygenase isozymes, with LOX3 being more frequently induced than LOX1. Foliar LOX3 activity was more frequently induced by M. caryaefoliae feeding in the moderately resistant ‘Oconee’ and highly resistant Money Maker and Cape Fear than in the susceptible genotypes. Therefore, the elevation of peroxidase is likely to be associated with aphid susceptibility and contributed to the severe leaf chlorosis, whereas the increase of LOX3 activity might be associated with aphid resistance in pecan. These findings contribute to our understanding of the etiology of M. caryaefoliae-elicited leaf chlorosis on pecan foliage. Such information may also be used to develop enzyme markers for identifying black pecan aphid resistance and/or susceptibility in pecan germplasm.

Abundance of volatile organic compounds in white ash phloem and emerald ash borer larval frass does not attract Tetrastichus planipennisi in a Y-tube olfactometer

Many natural enemies employ plant‐ and/or herbivore‐derived signals for host/prey location. The larval parasitoid Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) is 1 of 3 biocontrol agents currently being released in an effort to control the emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coloeptera: Burprestidae) in North America. To enhance its efficiency, allelochemicals that attract it need to be assessed. In this study, ash phloem volatile organic compounds (VOCs) of black, green, and white ash, and EAB larval frass were compared. Foraging behavior of T. planipennisi females in response to VOCs of white ash or frass from EAB larvae feeding on white ash phloem was tested using a Y‐tube olfactometer. Results indicated that the 3 ash species had similar VOC profiles. EAB larval frass generally contained greater levels of VOCs than phloem. Factor analysis indicated that the 11 VOCs could be broadly divided into 2 groups, with α‐bisabolol, β‐caryophyllene, (E)‐2‐hexenal, (Z)‐3‐hexenal, limonene, methyl benzoate, methyl indole‐3‐acetic acid, methyl jasmonate, methyl salicylate as the first group and the rest (i.e., methyl linoleate and methyl linolenate) as a second. Abundance of VOCs in white ash phloem tissue and frass, nevertheless, did not attract T. planipennisi females. The concealed feeding of EAB larvae might explain the selection for detectable and reliable virbrational signals, instead of undetectable and relatively unreliable VOC cues from phloem and frass, in short‐range foraging by T. planipennisi. Alternatively, it is possible that T. planipennisi is not amenable to the Y‐tube olfactometer assay employed.