1) Project title: Habitat affiliations of aphid-specialist enemies of Aphis glycines

Investigators: Michael Brewer, Takuji Noma, Matthew Kaiser and Shaun Langley, Michigan State University, Integrated Pest Management Program, Department of Entomology, B18 Food Safety and Toxicology Building, East Lansing, MI

Contact: Michael J. Brewer (brewerm@msu.edu)

Project description: Aphid-specialist enemies in soybean and surrounding habitats (alfalfa, corn, wheat-clover, and non-crop vegetation) were evaluated for their potential to attack Aphis glycines, the invasive soybean aphid. A substantial group of aphid-enemies, 8 parasitoids and 8 predatory flies, attacked A. glycines that were artificially placed in soybean and other habitats commonly found in soybean production areas. Habitat fidelity of the enemies varied. Of the parasitoids, Lysiphlebus testaceipes was the most common attacking A. glycines. It was found in most habitats including soybean and became abundant when A. glycines populations peaked. An undescribed Binodoxys (new species) was readily able to parasitize A. glycines, but almost exclusively in noncrop vegetation. And the parasitoid Aphelinus albipodus rarely parasitized A. glycines in all habitats visited but readily parasitized Rhopalosiphum padi on corn. Predatory flies as a whole more frequently attacked A. glycines than parasitoids. The cecidomyiid, Aphidoletes aphidimyza, was particularly abundant. Predatory flies were less habitat specific compared with parasitoids, although selected syrphid species appeared to have considerable habitat fidelity. Overall, the enemy fauna utilizing A. glycines on soybean was lower in species number (5 parasitoids and 6 predatory flies) and abundance for some species (up to 90% lower) compared with the enemy fauna utilizing A. glycines that was artificially placed in alfalfa, corn, wheat-clover, and non-crop vegetation.

2) Project title: Impact of soybean aphid chemical control on aphid enemies

Investigators:Takuji Noma and Michael Brewer, Michigan State University, Integrated Pest Management Program, Department of Entomology

Contact:Takuji Noma (noma@msu.edu)

Project description: Current soybean aphid management is largely limited to chemical control using broad-spectrum insecticides. With approximately 2 million acres of soybean production in Michigan, extensive insecticide use may increase risks of environmental contamination, poisoning of non-target organisms, and resistance development by pests. Another concern is the detrimental effect of insecticide applications on various natural enemies present in soybean fields. Impact of an insecticide application for soybean aphid control on aphid-specialist enemies was tested in July using replicated 1-acre soybean plots in Saginaw, Michigan. Four plots were treated with Warrior and other four plots were untreated when soybean plants were at R3 stage (beginning pod). Natural enemies (aphid parasitoids, aphid midges, and syrphids) were sampled one week after the insecticide application. Two types of sampling were employed in these plots: inspecting soybean plantings for direct observation of parasitoid mummies and immature predator flies, and placing pots of soybean plants infested with soybean aphids to attract ovipositing enemies. In both sampling methods, syrphids (complex of five species) were the most abundant natural enemies and parasitoids and aphid midges were relatively rare. The Warrior application significantly reduced syrphid populations by 91% compared with control populations, and 83% fewer syrphids were recovered from the potted plants placed in sprayed plots than in untreated plots. The results confirm adverse impact of insecticide on aphid-specialist enemies present in soybean fields.

3) Project title:The effect of a selective insecticide management program on natural enemies of the grape berry moth Endopiza viteana Clemens (Lepidoptera: Tortricidae).

Investigators: Paul E. Jenkins and Rufus Isaacs, Department of Entomology, Michigan State University.

Contact: Rufus Isaacs (isaacsr@msu.edu)

Project description: The grape berry moth (GBM), Endopiza viteana Clemens, is a primary pest of grapes in the eastern U.S. Recent registration of the insect growth regulator methoxyfenozide for use in grapes provides an opportunity for selective control of this key insect pest without disruption of biocontrol agents. The current project compares levels of GBM parasitism and natural enemy abundance in programs using methoxyfenozide for berry moth control to programs using conventional broad-spectrum insecticides. Two similarly sized vineyards (3.5-10 acres) at each of four commercial ‘Concord’ grape (Vitis labrusca) farms in southwest Michigan were selected for this study. Adult flight of male GBM was monitored in each treatment all season using pheromone traps to assess GBM phenology. Unbaited yellow sticky traps were deployed in each vineyard all season to monitor generalist natural enemies at each vineyard interior, vineyard border, and adjacent habitat border. In the selective insecticide treatment, applications of methoxyfenozide were based on weekly scouting and comparisons between programs were targeted at second and third GBM generations, when GBM pressure is highest. GBM infested berries were collected from both treatments to measure GBM larval parasitism. In the first two years of this study (2003 and 2004), the parasitism rate of GBM was found to be numerically greater in GBM infested berries collected from the methoxyfenozide-treated vineyards than in the conventional program. No significant difference in the abundance or community of natural enemies from yellow sticky trap collections was detected between treatments. Data from the third year of this study (2005) are still being analyzed.

4) Project title: The effect of agroecosystem modification on biological control agents of the grape berry moth Endopiza viteana Clemens (Lepidoptera: Tortricidae).

Investigators:Paul E. Jenkins and Rufus Isaacs, Department of Entomology, Michigan State University.

Contact:Rufus Isaacs (isaacsr@msu.edu)

Project description: The grape berry moth (GBM), Endopiza viteana Clemens, is a primary pest in eastern U.S. juice grape production. The ancestral host of this pest is wild grape (Vitis spp.). Recent research at MSU and grower experience suggests that removal of wild grape hosts in woodlots adjacent to vineyards may reduce GBM pressure. We are measuring the effect of this cultural control practice on the GBM parasitoid community and generalist natural enemy abundance within cultivated vineyards. One to ten acre paired-vineyards at five farms in southwest Michigan were used for this study. Wild grape in the woods adjacent to one of the vineyards was cut (to prevent fruiting), thereby removing a possible refuge for both GBM and their parasitoids. Adult flight of male GBM was monitored in each treatment all season using pheromone traps to assess GBM phenology. Unbaited yellow sticky traps were deployed in each treatment season-long to monitor generalist natural enemies at each vineyard interior, vineyard border, adjacent wood border, and wood interior. Infested berries were collected from both vineyards at each farm to measure GBM larval parasitism. In the first two years of this study (2003 and 2004), no significant difference was found in the number of parasitoids emerging from GBM infested berries between treatments. Additionally, there was not a significant treatment difference in the abundance or community of natural enemies from yellow sticky trap collections. Data from the last year of this three year study are currently being analyzed.

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5) Project title: Response of Natural Enemies to Reduced Use of Broad Spectrum Insecticide in Michigan Blueberry – Year 3

Investigators: K.S. Mason, M.E. O’Neal, C. Garcia-Salazar, J.C. Wise, and R. Isaacs, Department of Entomology, Michigan State University

Contact: Rufus Isaacs (isaacsr@msu.edu)

Project description: As part of a 4-year, USDA-RAMP funded project comparing pest management programs that employ either broad spectrum or reduced-risk insecticides, we measured abundance of natural enemies in the Michigan highbush blueberry agroecosystem. Two fields were chosen at each of six blueberry farms in southwest Michigan, one field received the grower’s standard insecticide program (GSTD) while the second received reduced-risk insecticides (RR). Yellow sticky traps, pitfall traps, tuna-baited test tubes, and periodic scouting were used in each field to test whether reduction in the use of broad-spectrum insecticides can increase generalist predator (coccinellid, syrphid, lacewing and spider), terrestrial arthropod predator (carabid beetles and formicid ants) or parasitoid abundance in RR plots. Results from this third year of this study suggest the rate of parasitism of blueberry aphid is higher in RR fields compared to that in GSTD fields, and ground foraging ant activity was greater in RR as compared to GSTD fields. The abundance of the carabid Harpalus erraticus in RR fields was greater than that in GSTD fields in 2003 and 2004, and a similar relationship was observed for another carabid, Amara aenea in 2004. Building on the observed differences in carabid abundances, we used exclusion cages to measure rates of predation on cranberry fruitworm and Japanese beetle in 2005. Results suggest carabids are important predators of these two key blueberry pests. In 2004 higher abundance of some generalist predators (coccinellids, spiders and ants) was observed in RR compared to GSTD fields. Similar data for 2005 are not analyzed, but early season results indicate there are differences in abundances of these predators between management programs. From this research, we hope to better understand the potential contribution of natural enemy populations to the control of major insect pests in blueberry.

6) Project title: A Comparison of Native Michigan and Nonnative Plants to Provide Resources to Natural Enemies

Investigators: Anna K. Fiedler and Douglas A. Landis, Dept. Entomology, Michigan State University.

Contact: Anna K. Fiedler, (fiedlera@msu.edu)

Project description: The use of plants to provide nectar and pollen resources to natural enemies via habitat management is a growing focus of conservation biological control. Most guidelines recommend annual plants not native to the area of study; there is, however, no a priori reason to suspect that native perennial plants cannot perform as well as non-native annuals.

During the 2004 and 2005 growing seasons, we compared of a set of forty-six native perennial Michigan and five non-native annual plants for their effectiveness as resource plants for natural enemies. We measured natural enemy abundance and insect diversity at peak bloom on 1 m2 of flowering plant material. We also measured a set of plant and flower characteristics: maximum flower height, flower color, floral area/ plot, and corolla depth and width, to determine which plant characteristics best correlate with natural enemy numbers per sample and whether any can be used as predictors for natural enemy attractiveness to plants.

In 2004, the previously recommended non-native plants Coriandrum sativum L., Vicia faba L., Fagopyron esculentum Moench, and Lobularia maritima (L.) Desv. (var. snow crystals) outperformed many of the native Michigan plants (Fig. 1). Exceptions were two native plant species that contained more natural enemies per sample than any non-native species at the same time: Heracleum maximum Bartr. and Eupatorium perfoliatum L. Other native plant species with high natural enemy numbers included Agastache nepetoides (L.) Kuntze, Aster novae-angliae L., and Solidago riddellii L. In year two, native perennial plants were more mature and, in contrast to 2004, the most attractive had consistently higher numbers of natural enemies per sample than the non-native plants (Fig.1).

We performed a multiple regression on the number of natural enemy arthropods per sample versus plant characteristics. In 2004, floral area was positively correlated with number of natural enemies per sample, explaining 31.1 percent of the variance (F=173.69, P<0.0001), and corolla width was negatively correlated with number of natural enemies, explaining an additional 1.75 percent of the variance (F=17.06, P<0.0001). Data from May-June 2005 show the same pattern, with floral area explaining 37.8 percent of the variation in natural enemy abundance (F=117.53, P<0.0001).

Our data indicate that the use of perennial plants in habitat management should be further investigated to increase the effectiveness of habitat management for conservation biological control.

7) Project title: Evaluating the Potential for Biological Control of Garlic Mustard in Michigan

Investigators:Jeffrey A. Evans¹, Adam S. Davis², Douglas A. Landis¹1, Douglas W. Schemske^3
1Department of Entomology, Michigan State University, East Lansing, MI 48824
²USDA ARS N-319 Turner Hall, 1102 S. Goodwin Ave., Urbana, IL 61801
³Department of Plant Biology, Michigan State University, East Lansing, MI 48824

Contact: Jeff Evans, (evansj18@msu.edu)

Project description: Garlic Mustard, Alliaria petiolata (Brassicaceae) (M. Bieb) Cavara and Grande, is an obligate biennial forb that is native to Europe, the Mediterranean region, and parts of Western Asia. It is invasive in North America and is now present and spreading in at least 34 U.S. States and 4 Canadian provinces. Alliaria petiolata is shade adapted and a aggressive competitor in forest understories, edge habitats, and disturbed areas. Established populations of A. petiolata set high numbers of seeds, and seeds can remain viable in the seed bank for up to five years. Conventional control methods have proven ineffective on all but the smallest infestations. Potential biological control organisms are currently under testing in Europe and in quarantine in the United States for host specificity and effectiveness.

We began taking baseline species composition data at eight A. petiolata infested sites representing a variety of forest types in the Lower Peninsula of Michigan to document the effects of changes in garlic mustard abundance on the existing community. Two parallel transects of ten 1m x 1m plots spaced 10m apart were established in April 2003 at each site, and percent garlic mustard coverage, species percent composition, percent coverage of plant, rock, and soil were recorded. All measurements have been repeated annually during fall and spring of 2003, 2004 and 2005 and will be take in future years. Transects at seven of eight sites were set up such that A. petiolata was not initially present in all 20 sampling quadrats thus allowing us to observe changes in its within-site distribution. Preliminary data analysis indicates that A. petiolata is expanding or maintaining its range at all sites (Figure 1) with insignificant herbivore damage.

A study of variability in Alliaria petiolata demography was initiated in June 2004. The first objective of this effort is to characterize spatial variability in A. petiolata demography. The second objective is to model the effects of potential biocontrol agents on A. petiolata populations across Michigan and determine whether single or multiple agent biocontrol will be necessary. Demographic parameters are being measured for A. petiolata populations at eight locations in southern Michigan representing a latitudinal and longitudinal gradient as well as both high and low levels of A. petiolata infestation. A model of A. petiolata demography will allow us to test the effectiveness of single and multiple biological control agents on A. petiolata across its Michigan range by applying varied levels of mortality at different stages in A. petiolata’s life cycle. Results from the first year of this study indicate that A. petiolata’s populations are spreading at all eight sites with population growth rates ( λ) ranging from 1.2 to 6.2. Values of λ greater than 1 indicate population expansion. Our calculated values of λ generally correspond to the high and low site infestation categories as predicted. Based on our current understanding of the level of mortality imposed on A. petiolata by the potential biocontrol agents and these initial data, our modeling predicts that five of the eight study sites may be amenable to intervention by biological control with single or multiple agent releases that impact rosette to flowering survival and fecundity.

In May, 2004 we established a factorial study to determine the joint effects of herbivore browsing and A. petiolata on native plants in forest understories. Plots with and without deer and turkey access and with our without A. petiolata were used to test the hypothesis that herbivores and A. petiolata negatively impact native plant communities, both separately and in concert. We marked 96 1m² permanent sampling quadrats in a high quality hardwood forest at the Edward Lowe Foundation’s Big Rock Valley in Cassopolis, MI. Sixty-four of the plots were set out in discrete patches of A. petiolata, and 32 plots were set out in areas completely free of A. petiolata (GM 0). Half of the plots containing A. petiolata plants were randomly assigned to have GM clipped at the root crown, bagged, and removed from the site (GM-) and half were left undisturbed (GM+). 16 randomly selected plots from each A. petiolata treatment were enclosed by a 1.5 m diameter, 1.5 m high wire mesh fence to exclude deer and turkeys (Deer-). Half of the remaining plots in each treatment were randomly assigned to receive a semicircle of the same material as a sham fence (Deer+) or no fencing (Deer0) as a cage control. Number of A. petiolata seedlings and adults and percent coverage of all other vegetation by species were recorded in each plot in June 2004. Changes in vegetation over time are expected to indicate effects of herbivore disturbance and/or A. petiolata invasion. Sampling of the site was repeated in May, June and September of 2005 and the A. petiolata removal treatments were maintained during the June sampling.

Figure 1. Count of sampling quadrats containing live A. petiolata plants during spring sampling. Alliaria petiolata has spread or maintained its distribution at all eight sites.

8) Project title: Relative impacts of natural enemy taxa on soybean aphid population regulation.

Investigators: Alejandro C. Costamagna and Douglas A. Landis, Dept. Entomology, Michigan State University.

Contact: Douglas A. Landis (landisd@msu.edu)

Project description: During 2005 we replicated a 2004 field experiment aimed at evaluating the joint impact of predators and parasitoids on A. glycines populations and examining the role of predators in limiting parasitoid impacts via intraguild predation (IGP). The experiment was conducted in the Biodiversity plots of the KBS-LTER site, Hickory Corners, Michigan. Using tomato cage frames covered with mesh we differentially excluded all natural enemies (< 1 mm mesh, Aphid treatment) or only large predators (2 mm mesh, Mesh treatment), thus allowing natural parasitism to occur protected from IGP by large predators. We also included un-caged plants with and without aphid manipulation (Open and Field treatments), plants enclosed with a sham cage (Sham treatment) as a cage control, and plants caged without aphids (Plant treatment). All cages and the open treatment were enclosed by a plastic cylinder coated on the outside with Tanglefoot to prevent ants from entering and tending aphids. Our preliminary results showed the same pattern as in 2004, with strong impacts from large predators (mainly Coccinellidae) but no control achieved by extant parasitoid populations or small predators (Fig. 1). During 2004 we had low levels of parasitism and we observed direct evidence of IGP (mummies being consumed), although parasitoids alone were ineffective in reducing aphid populations. During 2005, parasitoids were almost absent from our cages, even when protected from IGP. During 2004, large predator impacts on aphids resulted in a trophic cascade that significantly increased soybean height, biomass, and yield to similar levels than plants in which aphids were excluded. During 2005, a similar trend in plant height was observed (biomass and yield data not yet available). Our results show strong impacts of large predators on A. glycines during two consecutive years, and demonstrate a minor role of IGP in disrupting parasitism by the extant assemblage of A. glycines parasitoids.

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9) Project title: Impact of landscape complexity and intraguild interactions on predator community diversity and soybean aphid populations.

Investigators: Mary Gardiner and Doug Landis, 204 CIPS, Michigan State University, East Lansing, MI 48824

Contact: Mary Gardiner, (gardin18@msu.edu)

Project description:The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the North Central US since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse community of insect predators feed on soybean aphid throughout its invasive range. In the soybean growing regions of Michigan, Wisconsin, Minnesota and Iowa, landscape characteristics are likely to impact this community of natural enemies. To measure the effects of landscape complexity on aphid and natural enemy populations 13 sites throughout the North Central US were sampled. To relate arthropod populations to landscape complexity, aerial photographs were obtained for each site. A circle with a 3.5 radius originating from the center of each sampling site was digitized using ARC GIS 9. Using these digitized photographs, the land cover type of all areas within the circle were classified by visiting each location. From these maps, several landscape variables were calculated, including the proportion of land covered by soybean and the percentage of total crop and non-crop vegetation found. In 11 of the 13 sites, we found that predator communities were suppressing aphid population growth for some time during the growing season. In the remaining two populations high alate immigration caused aphid populations to be released from predator control. We are currently studying the impact of landscape variables on predator community diversity and abundance.

In the field, soybean aphid is fed upon by several predators, including the coccinellid Harmonia axyridis, the lacewing Chrysoperla carnea, and the aphid gall midge Aphidoletes aphidomyza which may also engage in intraguild predation. In particular, H. axyridis has been observed to feed the larvae of C. carnea and A. aphidomyza. Adult H. axyridis are transient predators, spending short feeding bouts within an aphid patch before flying to a new patch of aphids within or between soybean fields or to another crop. Larval stages of C. carnea or A. aphidomyza may spend their entire juvenile stage feeding on aphid colonies on a single plant or a few plants within a field. Since H. axyridis rarely removes all of the aphids within a patch, we hypothesized that if H. axyridis engages in intraguild predation of C. carnea and A. aphidomyza, the transient behavior of this lady beetle could cause aphid populations to escape overall control by natural enemies. We measured this impact by comparing aphid populations in a microcosm study. All microcosms consisted of three V1 soybean plants infested with 15 aphids/plant which were allowed to reproduce for two days after which they were assigned to 1 or 4 treatments: no predators, A. aphidomyza larvae or C. carnea larvae only, A. aphidomyza or C. carnea larvae + H. axyridis present for 3 hours, and microcosms exposed to 3 hours of H. axyridis feeding only. The ladybeetle was present for three hours to simulate its transient feeding behavior. When adult H. axyridis were present with larval A. aphidomyza or C. carnea, the ladybeetle did act as an intraguild predator. Despite intraguild feeding, aphid populations in microcosms with both predators did not differ significantly from aphid populations in microcosms with only C. carnea or A. aphidomyza present. Thus, the transient feeding behavior of Harmonia axyridis did not negatively impact aphid population control. Harmonia axyridis may also affect the foraging behavior of A. aphidomyza and C. carnea larvae, with both species exhibiting behavioral avoidance in the presence of this intraguild predator.

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2004-05 Publications (Brewer Lab)

Brewer, M. J., T. Noma, and N. C. Elliott. 2005. Hymenopteran parasitoids and dipteran predators of the invasive aphid Diuraphis noxia after enemy introductions: temporal variation and implication for future aphid invasions. Biol. Control, 33: 315-323.

Noma, T., M. J. Brewer, K. S. Pike, and S. D. Gaimari. 2005. Hymenopteran parasitoids and dipteran predators of Diuraphis noxia in the west-central Great Plains of North America: species records and geographic range. BioControl 50: 97-111.

2004-05 Publications (Landis Lab)

Journal Articles

Rutledge, C.E., R.J. O’Neil, T.B. Fox, and D.A. Landis. 2004. Soybean aphid predators and their use in IPM. Annals Ent. Soc. Am. 97: 240-248.

Menalled, F.D., D.A. Landis, and L.E. Dyer. 2004. Research and extension supporting ecologically based IPM systems. Journal of Crop Improvement 11 (1/2): 153-174.

Costamagna, A.C., and D.A. Landis. 2004. Effect of Food Resources on Adult Glyptapanteles militaris and Meteorus communis (Hymenoptera: Braconidae), Parasitoids of Pseudaletia unipuncta (Lepidoptera: Noctuidae). Environ. Entomol. 128-137.

Sebolt, D.C., and D. A. Landis. 2004. Arthropod Predators of Galerucella calmariensis L. (Coleoptera: Chrysomelidae): An assessment of biotic interference. Environ. Entomol. 356-361.

Landis. D.A., T.B. Fox, A.C. Costamagna. 2004. Impact of multicolored Asian lady beetle as a biological control agent. The American Entomologist. 50: 153-54.

Fox, T.B., D.A. Landis, F. F. Cardoso, C.D. DiFonzo. 2004. Predators suppress Aphis glycines Matsumura population growth in soybean. Environ. Entomol. 33: 608-618.

Costamagna, A.C., F.D. Menalled and D.A. Landis. 2004. Host density influences parasitism of the armyworm Pseudaletia unipuncta in agricultural landscapes. Basic and Applied Ecology. 5: 337-355.

Wilkinson, T.K., D.A. Landis, L.J. Gut. 2004. Parasitism of Obliquebanded Leafroller, Choristoneura rosaceana (Harris) (Lepidoptera:Tortricidae), in Commercially Managed Michigan Apple Orchards. J. Econ. Entomol. 97: 1524-1530.

O’Neal, M.E., E.L. Zontek, Z. Szendrei, D.A. Landis and R. Isaacs. 2005. Ground predator abundance affects prey removal in highbush blueberry (Vaccinium corymbosum) fields and can be altered by aisle ground covers. BioControl. 50:205-222.

O'Neal, M.E., D. A. Landis, E. Rothwell, L. Kempel, and D. Reinhard. 2005. Tracking Insects with Harmonic Radar: a Case-Study with Carabids in Annual Crop Habitat. The American Entomologist. 50: 212-218.

Fox, T.B., D.A. Landis, F.F. Cardoso and C.D. DiFonzo. 2005. Impact of predation on establishment of the soybean aphid Aphis glycines Matsumura in soybean, Glycine max L. BioControl. 50:545-563.

Landis, D.A., F.D. Menalled, F.D., A.C. Costamagna, and T.K. Wilkinson. 2005. Manipulating plant resources to enhance beneficial arthropods in agricultural landscapes. Weed Sci. 53:In Press

Book Chapters

Menalled, F.D., and D.A. Landis. 2004. Conservation of ground beetles in annual crops. p. 159-161 In J. Capinera (ed) Encyclopedia of Entomology Vol 1. Kluwer Academic Publishers. Dordrecht, The Netherlands.

Menalled, F.D., J.M. Alvarez and D.A. Landis. 2004. Molecular techniques and habitat manipulation approaches for parasitoid conservation in annual cropping systems. pp. 101-115 In G. Gurr & S. Wratten eds. Ecological Engineering for Pest Management. CSIRO Publishing Australia.

Wilkinson, T.K., and D.A. Landis. 2005. The role of plant resources and habitat diversification in biological control. Pp. 305-325 In F.L. Wäckers, P.C.J. van Rijn & J. Bruin eds. Plant Provided Food and Plant-Carnivore Mutualism. Cambridge University Press. Cambridge, UK.

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