Pest Of Small Grains Research Articles

Evaluation of Russian wheat resistance sources with the spectrum of South African Diuraphis noxia biotypes

AbstractRussian wheat aphid (RWA) Diuraphis noxia is a global pest of small grains, such as wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), oat (Avena L.), and rye (Secale L.). Though laborious and time‐consuming in terms of efforts required to eliminate the unwanted traits, wheat landraces have been widely used in breeding programs to deliver resistance sources and genes responsive to RWA among other stresses. Continuous exploitation of resistance traits/alleles in the landraces should be prioritized as a RWA intervention strategy to minimize its devastating impacts on wheat. Eighty donor lines were evaluated for their resistance to four South African RWA biotypes, namely RWASA1, RWASA2, RWASA3, and RWASA4. The collection was composed of 74 donor lines and six breeding lines collected from Afghanistan (38), Iran (22), Pakistan (11), United States (4), South Africa (2), Turkey (1), Georgia (1), and Egypt (1). Majority of the accessions were susceptible to RWASA3. Of the 80 accessions evaluated, 14 were uniformly resistant to moderately resistant to RWASA1, 9 to RWASA2, 7 to RWASA3, and 9 to RWASA4. A heterogeneous resistance (resistant–moderately resistant: ≥ 50%) was recorded in 18 accessions for RWASA1, 28 for RWASA2, 13 for RWASA3, and 17 for RWASA4. In addition, 25 genotypes performed comparably to the check genotype CItr 2401, with resistance to all four RWA biotypes. Selection of resistant lines for genetic improvement of RWA resistance is of paramount importance. The use of genotypes conferring both high levels and moderate resistance could offer scope for effective resistance to RWA in wheat. The merits of their exclusive resistance should be emphasized in prebreeding programs.

Greenbug, Schizaphis graminum (Rondani) (Insecta: Heteroptera: Aphididae)

The greenbug, Schizaphis graminum (Rondani), has been recognized as a major pest of small grains for over 150 years. Described by Rondani, it was first placed in the genus Aphis (Rondani 1852) and later moved to the genus Toxoptera. There are about 40 recognized Schizaphis species worldwide with seven known from North America (Blackman and Eastop 2000). This document is EENY-353, one of a series of the Entomology and Nematology Department, UF/IFAS Extension. Published: July 2005. 
 EENY-353/IN634: Greenbug, Schizaphis graminum (Rondani) (Insecta: Hemiptera: Aphididae) (ufl.edu)

Isolation of Early-Responsive MicroRNA From Diuraphis noxia (Hemiptera: Aphididae)-Resistant Wheat.

The Russian wheat aphid (Diuraphis noxia Kurdjumov) is an economically important pest of small grains in many countries. The past decades have seen the deployment of resistance-carrying wheat (Triticum aestivum L.) cultivars to control D. noxia. However, the emergence of resistance-breaking biotypes is negating this strategy. The role that noncoding RNA (ncRNA) molecules play in the wheat-D. noxia interaction has not been studied to date. This study aimed to isolate differentially regulated microRNA from a resistant and susceptible near-isogenic wheat line after aphid infestation. Twenty-seven identified miRNA were mostly related to stress-linked miRNA, and their predicted targets were linked with known D. noxia-feeding regulated proteins. These included transcription factors, signaling proteins, carbohydrate metabolism, and disease resistance pathways. Gene expression of three putative miRNAs and a predicted nucleotide-binding leucine-rich repeat gene with an identified miRNA target site in the NB-ARC domain displayed differential regulation between the resistant and susceptible plants. This study marks the initial investigation into understanding the role of ncRNA in a D. noxia-resistant wheat line after infestation and reports a correlation between a miRNA and its putative target for this interaction.

Cereal Leaf Beetle (Coleoptera: Chrysomelidae) Regional Dispersion and Relationship With Wheat Stand Denseness

Cereal leaf beetle, Oulema melanopus L., is a pest of small grains and the literature conflicts on whether it is more abundant in sparse or dense stands of wheat. Our objectives were to determine the impact of stand denseness on cereal leaf beetle abundance and to investigate the regional dispersion of cereal leaf beetles across North Carolina and Virginia. One-hundred twenty fields were sampled across North Carolina and Virginia during 2011 for stand denseness, and cereal leaf beetle eggs, larvae, and adults. Two small-plot wheat experiments were planted in North Carolina using a low and a high seeding rate. Main plots were split, with one receiving a single nitrogen application and one receiving two. Egg density, but not larva or adult density, was positively correlated with stand denseness in the regional survey. Furthermore, regional spatial patterns of aggregation were noted for both stand denseness and egg number. In the small-plot experiments, seeding rate influenced stand denseness, but not nitrogen application. In one experiment, egg densities per unit area were higher in denser wheat, while in the other experiment, egg densities per tiller were lower in denser wheat. Larvae were not influenced by any factor. Overall, there were more cereal leaf beetle eggs in denser wheat stands. Previous observations that sparse stands of wheat are more prone to cereal leaf beetle infestation can be attributed to the fact that sparser stands have fewer tillers, which increases the cereal leaf beetle to tiller ratio compared with denser stands.

Abiotic effects on the clear-winged grasshopper (Orthoptera: Acridae) and its fungal pathogen Entomophaga grylli (Entomophthorales: Entomophthoraceae) in an intermountain bunch-grass prairie

AbstractThe grasshopper, Camnula pellucida Scudder (Orthoptera: Acridae), is a severe pest of small grains and rangeland forage in North America. In a field experiment using cages containing C. pellucida in northwestern Montana, United States of America, we manipulated exposure to the fungal entomopathogen, Entomophaga grylli Fresenius (Entomophthorales: Entomophthoraceae) pathotype 1, temperature using small greenhouses, and moisture for the pathogen with water pillows. Treatment effects on fungal infection (mycosis) rates and grasshopper survivorship were assessed. Water pillows provided additional moist habitat for E. grylli without having an impact on grasshopper performance or the plant biomass and nitrogen content. Number of fungal spores, pathogen-induced mortality rates, and treatment effects on grass biomass and nitrogen content were also measured. Water pillows benefited the pathogen by increasing fungal spore levels by eightfold, which in turn shortened pathogen-exposed grasshopper survival time by half. In contrast, warming reduced fungal spore levels by 50% and subsequently reduced mortality from E. grylli by 67%. However, warmed pathogen-exposed grasshoppers did not exhibit enhanced survival, which may be due, in part, to intraspecific competition among the surviving grasshoppers.

Demographic parameters of Diuraphis noxia (Hemiptera: Aphididae) and Hippodamia variegata (Coleoptera: Coccinellidae) recorded in the context of D. noxia infesting resistant and susceptible cultivars of wheat

The Russian wheat aphid (RWA), Diuraphis noxia (Kurdjumov), is a serious pest of small grains and can cause losses of about 80% in wheat yields. Chemical control is ineffective against this pest so the combined use of host plant resistance and biological control is seen as a possible better means of controlling this pest. In this study, the potential effect of Omid (resistant) and Sardari (susceptible) cultivars of wheat on life table parameters and daily fecundity of RWA and its predator, Hippodamia variegata (Goeze), were determined using the age-stage two-sex life table theory. The results indicate that the rm, R0, λ, T and GRR of RWA were -0.005 ± 0.01 day-1, 0.9 ± 0.24 offspring per individual, 0.99 ± 0.01 day-1, 21.16 ± 1.79 days and 13.34 ± 2.91 offspring on Omid and 0.159 ± 0.01 day-1, 6.9 ± 0.54 offspring per individual, 1.17 ± 0.01 day-1, 12.14 ± 0.26 days and 12.73 ± 1.22 offspring on Sardari. The corresponding values for H. variegata fed on RWA reared on Omid were 0.24 ± 0.01 day-1, 399.35 ± 53.01 eggs, 1.27 ± 0.01 day-1, 24.67 ± 0.28 days and 544.23 ± 75.86 eggs and on Sardari 0.20 ± 0.006 day-1, 221.56 ± 34.68 eggs, 1.23 ± 0.01 day-1, 26.50 ± 0.41 days and 402.72 ± 67.55, respectively. The resistance of wheat cultivars significantly affected life table parameters and mean fecundity of RWA and H. variegata. Our results indicate that combining both host plant resistance and predators in the integrated pest management of RWA could result in a synergistic effect.

Biology and fertility life table of the greenbug, Schizaphis graminum (Hemiptera: Aphididae) on the resistant winter wheat cultivar (Pishgam) in Iran

The greenbug, Schizaphis graminum (Rondani) (Hemiptera: Aphididae) has been known as a major pest of small grains, particularly wheat, worldwide. In this study, the effect of new wheat cultivar (Pishgam) for cold regions on biological characteristics of greenbug was investigated in a greenhouse at 25 ± 2 °C, 55 ± 10% relative humidity and a photoperiod of 16:8 h (L:D). The raw data were analysed based on the age-stage, two-sex life table. The intrinsic rate of increase (r), the finite rate of increase (λ), the net reproduction rate (R0) and the mean generation time (T) of greenbug were 0.313 ± 0.0019, 1.36 ± 0.0027 females/female/day, 83.33 ± 0.331 females/female and 14.11 ± 0.09 days, respectively. The life expectancy of a nymph is 43.57 days. The maximum reproductive value of females is on the 16th day which coincides with the total pre-reproduction period counted from birth. Hence, the present results may provide helpful information for comprehensive IPM programme of greenbug on this variety in cold regions of Iran. Result revealed that nymphal survival rate of the aphid was 100% on studied cultivar like that on sensitive host plant cultivar.

Lethal and sublethal effects of direct exposure to acetamiprid on reproduction and survival of the greenbug, Schizaphis graminum (Hemiptera: Aphididae)

The acetamiprid, a neonicotinoid insecticide, is a popular crop-protection agent used in fields as well as in protected cultivation. The lethal and sublethal effects of acetamiprid on direct exposure to Schizaphis graminum (Rondani) (Hemiptera: Aphididae), a major pest of small grains, were tested under greenhouse condition. The intrinsic rate of natural increase (rm) value for the populations treated with LC30, LC50, LC60, LC70, LC80 concentrations of acetamiprid and distilled water as control was 0.1446 ± 0.01, 0.1842 ± 0.0144, 0.1979 ± 0.016, 0.1595 ± 0.0105, 0.0779 ± 0.0242, 0.3156 ± 0.0029; the net reproductive rate (R0) was 4.95 ± 0.63, 7.1 ± 1.19, 7.05 ± 1.16, 4.95 ± 0.77, 2.15 ± 0.53, 85.5 ± 2.53; the finite rate of increase (λ) was 1.1555 ± 0.0115, 1.2022 ± 0.0173, 1.2186 ± 0.0195, 1.1728 ± 0.0182, 1.0807 ± 0.026, 1.3711 ± 0.004; the gross reproduction rate was 7.26 ± 0.69, 9.92 ± 1.03, 9.28 ± 0.84, 5.79 ± 0.58, 2.96 ± 0.49, 85.5 ± 2.53: the mean generation time (T) was 11.13 ± 0.2, 10.72 ± 0.2, 9.94 ± 0.15, 10.1 ± 0.08, 10.23 ± 0.07, 14.1 ± 0.13, respectively. Also, cluster analysing clearly showed that Lethal and sublethal concentrations of acetamiprid has significant impact on reproduction and survival of S. graminum.

Polymorphisms in salivary‐gland transcripts of Russian wheat aphid biotypes 1 and 2

Abstract The Russian wheat aphid (RWA), Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), is a major pest of small grains. As with plant‐feeding aphids in general, the interaction between RWA and host plants is governed, on the insect side, by proteins and enzymes in saliva. In this work, we examined sequence variations in transcripts encoding proteins and enzymes of RWA salivary glands. We conducted reverse transcription – polymerase chain reaction in RWA biotypes 1 and 2 using primers derived from pea aphid orthologs, and cloned regions of 17 putative salivary gland transcripts. For four of the transcripts, we observed no difference in sequences between the two biotypes. For the other 13 transcripts, for example, the transcripts encoding sucrase, trehalase and protein C002, large amount of variations, both within each biotype and between the two biotypes, were observed. Usually the two biotypes shared only one variant, which was typically the most common variant in both biotypes. Most of the transcripts had more non‐synonymous than synonymous codon changes among their variants. Our results offer possible molecular markers for distinguishing the two biotypes and insights into their evolution.

Diuraphis noxiaReproduction and Development With a Comparison of Intrinsic Rates of Increase to Other Important Small Grain Aphids: A Meta-Analysis

The Russian wheat aphid, Diuraphis noxia (Kurdjumov), is a significant pest of small grains in the United States and worldwide. There is an increasing need for quality population dynamic models to aid in development of integrated pest management strategies. Unfortunately, there exists high variability in published data regarding basic life history traits that frequently direct model parameterization. Metadata were analyzed to develop relationships between temperature and reproductive and developmental traits of D. noxia. Specifically, functions were developed between temperature and the following traits: lifespan, fecundity, fecundity rate, pre-nymphipositional period, reproductive period, and intrinsic rate of increase. Lower and upper temperature reproductive thresholds were calculated as 0.6 and 36.9 degrees C, respectively. The lower temperature developmental threshold was calculated as -0.69 degrees C. Modeled longevity reached its maximum at approximately 80 d. Meta-analysis indicates maximum fecundity at approximately 18.5 degrees C, with a maximum fecundity rate of approximately 2.1 nymphs per day over the nymphipositional period. The calculated maximum total fecundity was approximately 55 nymphs per female. The maximum reproductive period was calculated to be 29.9 d. Compared with other aphid species, as temperature increased, the intrinsic rate of increase of D. noxia increased more slowly relative to Schizaphis graminum (Rondani) and Rhopalosiphum padi L., but at a similar rate to Sitobian avenae (F.).

Effect of Biotype and Temperature on Fitness of Greenbug (Hemiptera: Aphididae) on Sorghum

The greenbug, Schizaphis graminum (Rondani) (Hemiptera: Aphididae), is a major aphid pest of small grains and sorghum, Sorghum bicolor (L.) Moench. Greenbugs extract juice and inject toxin, killing seedlings or limiting the yield of older plants. Understanding greenbug biology and how biotypes develop is important for evaluating and developing sorghum with durable resistance. Prereproductive period, fecundity, and longevity of greenbug biotypes E and I were assessed on susceptible 'RTx430' sorghum at four cycling temperatures of 10-23, 14-27, 18-31, and 22-35 degrees C in an incubator. A photoperiod of 14:10 (L:D) h corresponded with daily warm and cool temperatures. Greenbug fitness was more affected by temperature than biotype. Greenbug prereproductive period, total fecundity, and longevity did not differ among temperature regimes except at the warmest regime (22-35 degrees C), at which all parameters were greater for biotype E than biotype I. The prereproductive period of greenbug biotypes E and I combined was more than twice as long at the coolest temperature of 10-23 degrees C as at 22-35 degrees C. Greenbugs produced a maximum average of 3.3 more nymphs per day at warmer than cooler temperature regimes. Average total fecundity was greatest at 10-23 degrees C, with fewest nymphs being produced at 22-35 degrees C. Longevity of greenbug biotypes E and I combined was 6 times longer at 10-23 degrees C than at 22-35 degrees C. This study provides information on optimal temperatures under which to evaluate damage to sorghum being developed for resistance to different biotypes ofgreenbug.

Grain and Vegetative Biomass Reduction by the Russian Wheat Aphid1in Winter Wheat

The Russian wheat aphid, Diuraphis noxia (Mordvilko), is a severe pest of wheat, Triticum aestivum L; barley, Hordeum vulgare L; other small grains; and grasses. Although the Russian wheat aphid is a significant pest of small grains, its feeding effects on grain yield and vegetative biomass in large-scale wheat fields have not been well documented. Data were collected for 3 years in dryland and irrigated wheat fields in Texas and Oklahoma. The insect reduced grain yield 50.2 to 82.9% and biomass by 55.4 to 76.5%. These results suggested that winter wheat suffers significant economic loss from Russian wheat aphid.

Reproduction and Development of Russian Wheat Aphid Biotype 2 on Crested Wheatgrass, Intermediate Wheatgrass, and Susceptible and Resistant Wheat

The Russian wheat aphid, Diuraphis noxia (Kurdjumov), is an economically important pest of small grains. Since its introduction into North America in 2003, Russian wheat aphid Biotype 2 has been found to be virulent to all commercially available winter wheat, Triticum aestivum L., cultivars. Our goal was to examine differences in Russian wheat aphid reproduction and development on a variety of plant hosts to gain information about 1) potential alternate host refuges, 2) selective host pressures on Russian wheat aphid genetic variation, and 3) general population dynamics of Russian wheat aphid Biotype 2. We studied host quality of two wheatgrasses (crested wheatgrass, Agropyron cristatum [L.] Gaertn., and intermediate wheatgrass, Agropyron intermedium [Host] Beauvoir) and two types of winter wheat (T. aestivum, one Biotype 2 susceptible wheat, ‘Custer’ and one biotype 2 resistant wheat, STARS02RWA2414-11). The susceptible wheat had the highest intrinsic rate of increase, greatest longevity and greatest fecundity of the four host studied. Crested wheatgrass and the resistant wheat showed similar growth rates. Intermediate wheatgrass had the lowest intrinsic rate of increase and lowest fecundity of all tested hosts.

Reproduction and Development of Russian Wheat Aphid Biotype 2 on Crested Wheatgrass, Intermediate Wheatgrass, and Susceptible and Resistant Wheat

The Russian wheat aphid, Diuraphis noxia (Kurdjumov), is an economically important pest of small grains. Since its introduction into North America in 2003, Russian wheat aphid Biotype 2 has been found to be virulent to all commercially available winter wheat, Triticum aestivum L., cultivars. Our goal was to examine differences in Russian wheat aphid reproduction and development on a variety of plant hosts to gain information about 1) potential alternate host refuges, 2) selective host pressures on Russian wheat aphid genetic variation, and 3) general population dynamics of Russian wheat aphid Biotype 2. We studied host quality of two wheatgrasses (crested wheatgrass, Agropyron cristatum [L.] Gaertn., and intermediate wheatgrass, Agropyron intermedium [Host] Beauvoir) and two types of winter wheat (T. aestivum, one Biotype 2 susceptible wheat, 'Custer' and one biotype 2 resistant wheat, STARS02RWA2414-11). The susceptible wheat had the highest intrinsic rate of increase, greatest longevity and greatest fecundity of the four host studied. Crested wheatgrass and the resistant wheat showed similar growth rates. Intermediate wheatgrass had the lowest intrinsic rate of increase and lowest fecundity of all tested hosts.

Cereal leaf beetle: is performance affected by grass endophytes?

Cereal leaf beetle (CLB), Oulema melanopus (L.) (Coleoptera: Chrysomelidae), a long known pest of small grains in Europe, was first recorded in North America (Michigan) in 1962.

Biotypic Variation Among North American Russian Wheat Aphid (Homoptera: Aphididae) Populations

The Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), has been a major economic pest of small grains in the western United States since its introduction in 1986. Recently, a new Russian wheat aphid biotype was discovered in southeastern Colorado that damaged previously resistant wheat, Triticum aestivum L. Biotype development jeopardizes the durability of plant resistance, which has been a cornerstone for Russian wheat aphid management. Our objective was to assess the relative amount of biotypic diversity among Russian wheat aphid populations collected from cultivated wheat and barley, Hordeum vulgare L. We conducted field surveys from May through June 2002 and August 2003 from seven counties within Texas, Kansas, Nebraska, and Wyoming. Based upon a foliar chlorosis damage rating, three new Russian wheat aphid biotypes were identified, one of which was virulent to all characterized sources of Russian wheat aphid resistance. The future success of Russian wheat aphid resistance breeding programs will depend upon the continual monitoring of extant biotypic diversity and determination of the ecological and genetic factors underlying the development of Russian wheat aphid biotypes.

Inheritance of resistance to the Russian wheat aphid in an Iranian durum wheat line

AbstractThe Russian wheat aphid (RWA), Diuraphis noxia (Mordvilko), is a major economic pest of small grains in many countries. An experiment was therefore conducted to determine the inheritance of gene(s) controlling resistance to RWA in a resistant tetraploid durum wheat line. This resistant line,‘1881′, was crossed to a susceptible line, ‘Orejy‐e‐Kazeroon’, and then F1 F2 and BCF1 (backcross to susceptible line) seedlings were screened in a greenhouse for RWA resistance following artificial infection. Resistance in ‘1881’ was apparently controlled by one dominant gene. Since Dnl, Dn2, dn3, Dn4 and Dn5 have been reported to be located on genome D, it was reasoned that the resistance gene in ‘1881’ is not allelic to them.

Relationship between cereal leaf beetle (Coleoptera: Chrysomelidae) egg and fourth-instar populations and impact of fourth-instar defoliation of winter wheat yields in North Carolina and Virginia.

Cereal leaf beetle, Oulema melanopus (L.), has become a serious pest of small grains in the mid-Atlantic region of the United States. Existing thresholds for implementing control measures allowed too much leaf damage and consequent yield loss to occur before recommending treatment. Information on beetle biology and crop response to injury, both prerequisites for developing new management strategies, was lacking for this region. A 3-yr project was initiated to generate an area wide cereal leaf beetle biological and yield impact database for winter wheat, and to evaluate the injury and yield loss potential of different population densities. Over the study period, beetle populations were evaluated at 26 winter wheat field locations in Virginia and North Carolina. Eggs and larvae, classified to instar, were counted twice each week from February to June. Replicated insecticide versus noninsecticide treatments were conducted at each location where leaf defoliation and yield were documented. Results showed that the relationship between 50th percentile egg and fourth-instar population estimates were in strong agreement (y = 0.36x - 0.01; r2 = 0.79). Potentially detrimental larval infestations were forecast before appearance of foliage injury from egg populations present during the stem elongation to flag leaf emergence developmental stages. A significant positive linear relationship between total fourth instar per stem population estimates and percent flag leaf defoliation was detected (y = 20.29x + 1.34; r2 = 0.60). A weaker but still significant relationship between the total fourth-instar population estimates and percent yield loss was found (y = 11.74x + 6.51; r2 = 0.26), indicating that factors in addition to flag leaf injury, primarily by fourth instars, also contributed to reduced yields.

Inheritance and allelic relationships of resistances to the Russian wheat aphid in two Iranian wheat lines

Russian wheat aphid (RWA), Diuraphis noxia (Kurdjumov), is a serious pest of small grains in many countries. A previous study screened 70 genotypes, collected from different parts of Iran, for RWA resistance. Four crosses were made between two resistant lines (Shz.W-102 and Shz.W-104) and two susceptible lines (Shz.W-101 and Shz.W-103). Parents, F1, F2, and BCF1 seedlings were screened for RWA resistance in the greenhouse by artificial infection. To determine allelism, the two resistant lines were intercrossed and F1, and F2 seedlings were evaluated. Resistance in Shz.W-102 and Shz.W-104, when crossed with Shz.W-101, was controlled by one dominant gene. However, resistance in Shz.W-102 and Shz.W-104, when crossed with Shz.W-103, was controlled by two dominant genes. Genes in two resistant lines segregated independently of each other. A three-gene system was proposed to govern resistance in the lines under study .

Aphelinus albipodus(Hymenoptera: Aphelinidae) andDiaeretiella rapae(Hymenoptera: Braconidae) Parasitism onDiuraphis noxia(Homoptera: Aphididae) Infesting Barley Plants Differing in Plant Resistance to Aphids

Russian wheat aphid,Diuraphis noxia(Mordvilko), as a pest of small grains, has prompted research into biological control and host plant resistance. In the presence of Russian wheat aphid, leaves of a susceptible barley (Morex) are curled and chlorotic and sustain large densities of this aphid, while leaves of a resistant barley (STARS-9301B) remain flat and green and sustain fewer aphids. Might parasitism of Russian wheat aphid byAphelinus albipodusHayat & Fatima andDiaeretiella rapaeMcIntosh be affected differently by these plant types? When presented the plants separately and based on parasitism rate relative to aphid density, the largerD. rapaewas more effective in parasitizing relatively high densities of aphids within curled leaves of Morex than relatively low densities of aphids on uncurled leaves of STARS-9301B. Parasitism byA. albipodusdid not significantly differ among the plants. When given a choice of plants, approximately equal rates of parasitism occurred on the two plant lines for both parasitoid species, and parasitism byD. rapaewas greater thanA. albipodus.These data indicate that using parasitoid size as an indicator of success in a physically restricted environment may be misleading, when considered in a plant environment responsive in several manners to aphids (chlorosis, curling, and ability to sustain Russian wheat aphid). We expect that use of resistant barley will result in decreased parasitoid abundance as aphid densities decrease. However, parasitism rates are expected to be approximately equal on resistant and susceptible barley. In this system, plant resistance and biocontrol are compatible management strategies.