Characterization of Stink Bug (Heteroptera: Pentatomidae) Damage to Mid- and Late-Season Apples 1,2

Similar documents
BMSB Small Fruit Stakeholder Report

Peach and Nectarine Cork Spot: A Review of the 1998 Season

Status of Halyomorpha halys in the Mid-Atlantic U.S. Tom Kuhar Professor and Vegetable Entomology Specialist Department of Entomology, Virginia Tech

SYMPTOMS OF CONTROLLED ATMOSPHERE DAMAGE IN AVOCADOS

Progress Report Submitted Feb 10, 2013 Second Quarterly Report

USDA. Project: Brown Marmorated Stink Bug: Damage Survey and' Monitoring Efforts

Journal of Economic Entomology Advance Access published February 8, 2015

Studies in the Postharvest Handling of California Avocados

(36) PROHEXADIONE-CALCIUM AFFECTS SHOOT GROWTH AND YIELD OF LEMON, ORANGE AND AVOCADO DIFFERENTLY

Effects of Preharvest Sprays of Maleic Hydrazide on Sugar Beets

THE EFFECT OF ETHYLENE UPON RIPENING AND RESPIRATORY RATE OF AVOCADO FRUIT

TEMPERATURE CONDITIONS AND TOLERANCE OF AVOCADO FRUIT TISSUE

GALA SPLITTING WASHINGTON TREE FRUIT POSTHARVEST CONFERENCE. March 13 th & 14 th, 2001, Wenatchee, WA PROCEEDINGS, Gala Splitting page 1 of 6

Tom Kuhar & D. Ames Herbert Dept. of Entomology Virginia Tech

Spotted wing drosophila in southeastern berry crops

Southern Green Stink Bug, Nezara viridula (L.),

Effect of Storage Period and Ga3 Soaking of Bulbs on Growth, Flowering and Flower Yield of Tuberose (Polianthes Tuberosa L.) Cv.

Flowering and Fruiting Morphology of Hardy Kiwifruit, Actinidia arguta

Life Cycle. Objective 2/16/2015. Brown Marmorated Stink Bugs and Common Look-Alikes

Proceedings of The World Avocado Congress III, 1995 pp

Identification. Adults may be confused with other native brown stink bugs and western conifer seed bugs.

Lygus: Various Species Monitoring Protocol

A new approach to understand and control bitter pit in apple

COMPARISON OF CORE AND PEEL SAMPLING METHODS FOR DRY MATTER MEASUREMENT IN HASS AVOCADO FRUIT

Calcium Use in Apples: An Update. M. Elena Garcia, PhD

NEW ZEALAND AVOCADO FRUIT QUALITY: THE IMPACT OF STORAGE TEMPERATURE AND MATURITY

BIO-EFFICACY OF NEWER INSECTICIDES AGAINST POD BORER COMPLEX OF PIGEONPEA [Cajanus cajan (L.) Millspaugh] *PATEL, S. A. AND PATEL, R. K.

Citrus Canker and Citrus Greening. Holly L. Chamberlain Smoak Groves AGRI-DEL, INC. Lake Placid, FL

2009 Barley and Oat Trials. Dr. Heather Darby Erica Cummings, Rosalie Madden, and Amanda Gervais

Diagnosing Vegetable Problems

PERFORMANCE OF HYBRID AND SYNTHETIC VARIETIES OF SUNFLOWER GROWN UNDER DIFFERENT LEVELS OF INPUT

Michigan Grape & Wine Industry Council 2012 Research Report. Understanding foliar pest interactions for sustainable vine management

Further investigations into the rind lesion problems experienced with the Pinkerton cultivar

UNIVERSITY OF CALIFORNIA AVOCADO CULTIVARS LAMB HASS AND GEM MATURITY AND FRUIT QUALITY RESULTS FROM NEW ZEALAND EVALUATION TRIALS

Apples. References: New York Apple Association, Rutgers University, University of Georgia, Washington Apple Commission.

Relationship between Mineral Nutrition and Postharvest Fruit Disorders of 'Fuerte' Avocados

NAME OF CONTRIBUTOR(S) AND THEIR AGENCY:

Managing Spotted Wing Drosophila, Drosophila Suzukii Matsumara, In Raspberry.

Sweet corn insect management by insecticides in Ohio, 2015 Final report 12/31/2015

Response of 'Hass' Avocado to Postharvest Storage in Controlled Atmosphere Conditions

Takao IcHli and Kenichi HAMADA Faculty of Agriculture, Kobe University, Kobe and Agricultural Experiment Station of Hyogo Prefecture, Sumoto

YIELD, CULTURAL PRACTICES AND YIELD LIMITING FACTORS

BEEF Effect of processing conditions on nutrient disappearance of cold-pressed and hexane-extracted camelina and carinata meals in vitro 1

Stink Bugs and Leaffooted Bugs Are Important Fruit, Nut, Seed and Vegetable Pests 1

Olives Postharvest Quality Maintenance Guidelines. Carlos H. Crisosto and Adel A. Kader Pomology Department University of California Davis, CA 95616

Ripening, Respiration, and Ethylene Production of 'Hass' Avocado Fruits at 20 to 40 C 1

Fungicides for phoma control in winter oilseed rape

Pecan Production 101: Sunlight, Crop Load Management, Pollination. Lenny Wells UGA Extension Horticulture

Managing Insect Pests of Ripening Grapes

CORRELATIONS BETWEEN CUTICLE WAX AND OIL IN AVOCADOS

Southern Region Small Fruit Consortium Final Report Title: Final Report Grant Code: Research Project Personnel: Objectives: Justification:

Topics to be covered: What Causes Fruit to Rot? Powdery Mildew. Black Rot. Black Rot (Continued)

STORAGE SCALD OF APPLES

Michigan Grape & Wine Industry Council 2008 Research Report

Project Title: Testing biomarker-based tools for scald risk assessment during storage. PI: David Rudell Co-PI (2): James Mattheis

IMPACT OF RAINFALL PRIOR TO HARVEST ON RIPE FRUIT QUALITY OF HASS AVOCADOS IN NEW ZEALAND

Citrus. Disease Guide. The Quick ID Guide to Emerging Diseases of Texas Citrus. Citrus. Flash Cards. S. McBride, R. French, G. Schuster and K.

Citrus Crop Guide. New registration for citrus gall wasp

Hybrid Seeds Production

Assessment of Specialty Potatoes for Powdery Scab Resistance

Research - Strawberry Nutrition

ALTERNATIVE CONTROL METHODS FOR GRAPE LEAFHOPPER: PART 2 FINAL REPORT 1/22/01

The Pomology Post. Hull Rot Management on Almonds. by Brent Holtz, Ph.D., University of California Pomology Advisor

THE EFFECT OF GIRDLING ON FRUIT QUALITY, PHENOLOGY AND MINERAL ANALYSIS OF THE AVOCADO TREE

MANAGING INSECT PESTS IN BERRIES AND FRUITS. Small Farm School 8 September 2012 Bruce Nelson, CCC Horticulture Department

Smoke Taint Update. Thomas Collins, PhD Washington State University

Managing potato leafhopper in wine grapes

Using Growing Degree Hours Accumulated Thirty Days after Bloom to Help Growers Predict Difficult Fruit Sizing Years

INFESTATION PATTERN OF Scirtothrips dorsalis Hood (THYSANOPTERA : THRIPIDAE) IN DEVELOPING SHOOT AND FLOWER OF MANGO ARUMANIS 143

POTATOES USA / SNAC-INTERNATIONAL OUT-OF-STORAGE CHIP QUALITY MICHIGAN REGIONAL REPORT

Almond & Walnut Harvest Evaluation: Identifying Sources of Damage

Evaluation of Compost Teas for Disease Management of Wild Blueberries in Nova Scotia

The Invasive Brown Marmorated Stink Bug In Utah Halyomorpha halys

Southern Region Small Fruit Consortium Progress Report Title: Progress Report Grant Code: Research Project Personnel: Objectives:

How to Identify and Manage Brown Marmorated Stink Bug (Halyomorpha halys)

Objective: To examine Romaine lettuce varieties for resistance to yellow spot disorder

Evaluation of Insect-Protected and Noninsect-Protected Supersweet Sweet Corn Cultivars for West Virginia 2014

Is fruit dry matter concentration a useful predictor of Honeycrisp apple fruit quality after storage?

Evaluation of 17 Specialty Pepper Cultivars in Southwest Michigan

Physiological Gradient in Avocado Fruit

ORGANIC MANGO CROP PROTECTION PART-III post harvest care, physiological disorders & micronutrient deficiencies ICCOA, BANGALORE

THE THREAT: The disease leads to dieback in shoots and fruiting buds and an overall decline in walnut tree health.

Evaluation of Caffeine and Garlic Oil as Bird Repellents

GRAIN SORGHUM. Tifton, Georgia: Early-Planted Grain Sorghum Hybrid Performance, 2012 Nonirrigated. 2-Year Average Yield

INFLUENCE OF ENVIRONMENT - Wine evaporation from barrels By Richard M. Blazer, Enologist Sterling Vineyards Calistoga, CA

PGR Strategies to Increase Yield of Hass Avocado

What went wrong. Pepper Sunscald. In this issue, find out what might have gone wrong with your vegetable harvest this season.

CARIBBEAN FOOD CROPS SOCIETY

Stella Maris on Wine Grapes. Spring, 2018

EFFECT OF FRUCOL APPLICATION ON SHELF LIVE OF IDARED APPLES

2003 NEW JERSEY HEIRLOOM TOMATO OBSERVATION TRIAL RESULTS 1

APPENDIX Thirty Trees Sampling Method for CBB Monitoring

The Benefits of Insecticide Use: Avocados

Midwest Cantaloupe Variety Trial in Southwest Indiana 2015

Experimentation to Monitor and Control Grape Root Borer. Martin Keen Landey Vineyards Lancaster, PA

Information sources: 1, 5

Fruit Ripening & Retail Handling Workshop. Why use cold storage? Ripe Strawberries After 7 days. Respiration and Temperature.

Effect of Inocucor on strawberry plants growth and production

Quality of western Canadian flaxseed 2012

Use of Plant Growth Regulators to Increase Fruit Set, Fruit Size and Yield and to Manipulate Vegetative and Floral Shoot Growth

Transcription:

Characterization of Stink Bug (Heteroptera: Pentatomidae) Damage to Mid- and Late-Season Apples 1,2 Mark W. Brown U. S. Dept. Agriculture, Agricultural Research Service, Appalachian Fruit Research Station, 2217 Wiltshire Rd., Kearneysville, West Virginia 25430 USA J. Agric. Urban Entomol. 20(4): 193 202 (October 2003) ABSTRACT Stink bugs (Heteroptera: Pentatomidae) were found to feed on apples in mid- to late season, from late July until harvest. Stink bug-feeding damage has been confused with cork spot, but differs in three ways: 1) the edge of the depression on the fruit surface from stink bug feeding is gradual instead of abrupt as in cork spot, 2) the corky flesh is always immediately beneath the skin in stink bug damage but may not be in contact with the skin in cork spot, and 3) the presence of a puncture site from stink bug feeding. Application of foliar calcium chloride did not affect the occurrence of corking damage related to stink bug feeding, and the fruit flesh immediately below the skin in stink bug damaged fruit had the same concentration of calcium and boron as fruit flesh from undamaged fruit. Damage caused by stink bugs was eliminated by caging fruit in early July, whereas damage was higher on fruit caged with stink bugs for a two-week period between late July and harvest than on fruit that were not caged. Most stink bug damage occurred from 26 to 60 days before harvest. KEY WORDS Pentatomidae, calcium chloride, boron, cork spot, bitter pit Stink bugs (Heteroptera: Pentatomidae) are well-known pests of rice (Bowling 1979), legumes (Nilakhe et al. 1981), nuts (Yates et al. 1991, Shearer & Jones 1996), and fruits (Mundinger & Chapman 1932, Borden et al. 1952). Feeding on seeds or the fruiting structures surrounding seeds of these and other crops causes economic damage. Stink bugs penetrate the plant s protective structures to feed through a combination of mechanical pressure exerted by the mouthparts and saliva-containing enzymes that dissolve components of the cell wall and intercellular matrix (Miles 1958, Miles 1959). Damage to temperate, deciduous tree fruit appears as two different defects. Feeding on apple early in the season causes a dimple on the surface of the fruit with a trail into the fruit flesh toward the seeds or calyx (Solymar 1999). In peaches, early damage develops into cat-facing injury, as a result of the surrounding undamaged fruit flesh growing around the damaged feeding site (Rings 1958). Later season damage to peach appears as a depressed area on the fruit surface, a water-soaked lesion, or gummosis (Rings 1 Accepted for publication 16 April 2004. 2 This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the USDA for its use. 193

194 J. Agric. Urban Entomol. Vol. 20, No. 4 (2003) 1958), apparently as a result of loss of cell contents from many cells (Mundinger & Chapman 1932). In peaches and pear, the flesh has a white or brown, pithy appearance (Mundinger & Chapman 1932) but in apple the damaged flesh is brown and corky (Krupke & Brunner 2001). In eastern North America, mid to late season stink bug damage has been reported in peach and pear, but generally has not been considered to be an economic problem for apple (Mundinger & Chapman 1932, Solymar 1999). Disorders associated with nutrient deficiencies in apple, especially cork spot and bitter pit, can be confused with stink bug feeding (Brown 2001a). In particular, calcium-related deficiency can cause symptoms that include a corky appearance of apple flesh under a depressed and discolored area on the fruit skin (Faust & Shear 1968). The variety York Imperial is especially susceptible to a corking disorder (Simons et al. 1971, Miller 1980) that is related to calcium deficiency. A number of studies (Faust & Shear 1968, Shear 1972, Raese & Drake 1993) have demonstrated that the application of foliar calcium can reduce the occurrence of this disorder in apple. Other factors such as crop load, defoliation, water relations, and storage conditions also can contribute to cork spot and bitter pit development (Faust & Shear 1968). This study was conducted to characterize stink bug feeding damage to apples during the mid-season to harvest stages of fruit development. Experiments were conducted to determine if the observed damage could be prevented by excluding stink bugs and to eliminate the possibility of calcium deficiency as a contributing cause. Materials and Methods Experimental orchard. Experiments on stink bug feeding damage to apple were superimposed on an existing study examining the effect of increasing plant diversity on arthropod pest management conducted at the Appalachian Fruit Research Station, Kearneysville, West Virginia (Brown 2001b). Four 0.5-ha orchards were planted in April 1997 with Loring /Lovell peach (Prunus persica Batsch), and Granny Smith /EMLA.26 and Royal Empire /M.9/EMLA.111 apple (Malus x domestica Borkh.) at a spacing of 3.7 4.9 m (560 trees/ha). The control (C) orchard was planted with a contiguous block of peach adjacent to a contiguous block of apple. The interplanted (I) orchard was planted with alternating pairs of apple and peach trees within and among tree rows. The ground cover (GC) orchard was planted with contiguous plantings of apple and peach as in orchard C. Alternating strips of dill (Anethum graveolens L.), buckwheat (Fagopyrum esculentum Moench), purple tansy (Phacelia tanacetifolia Benth.), and a mixture of 16 wildflowers (partial shade mix, American Meadows, Williston, Vermont) were planted under each side of the tree row in 0.75-m wide strips extending from 1.25 to 2.00 m from the center line of the row. The final orchard, interplanted/ground cover (I/GC), had the highest plant diversity combining interplanting of fruit trees and flowering annual plants under the trees as described above. Orchard C was treated with a conventional insecticide application schedule, and the other three orchards received a reduced insecticide schedule (Table 1). Cage studies. Thirty individual branches of each apple cultivar were caged with 10 50 threads/cm screen (BioQuip Products, Gardena, California) to ex-

BROWN: Stink Bug Damage to Apples 195 Table 1. Insecticide treatments in conventional and reduced program orchards for characterizing stink bug damage to apple fruit, Kearneysville, West Virginia, 2001. Date Conventional program Reduced program May 8 Indoxacarb Indoxacarb May 17 Phosmet Bacillus thuringiensis June 4 Phosmet June 20 Methomyl July 2 Methomyl July 27 Esfenvalerate August 16 Phosmet September 18 Phosmet clude insects after 11 July 2001. Branches were pruned before caging so that at least five fruit were within each 1.0-m long by 0.5-m diameter cage. Six cages per cultivar were randomly assigned to one of five treatments, four receiving two stink bugs for approximately two-week periods and one a control with no stink bugs. Exposure to stink bugs on Empire branches was 48 to 36 days, 35 to 26 days, 25 to 16 days, and 15 to 0 days before harvest (7 September 2001). Exposure to stink bugs on Granny Smith branches was 60 to 46 days, 45 to 32 days, 31 to 18 days, and 17 to 0 days prior to harvest (16 October 2001). Stink bugs were field collected in Jefferson County, West Virginia, during the summer and maintained in laboratory cages containing a mixture of flowering annual plants. Cages were kept in a growth chamber at 16:8 (L:D) photoperiod at 24 26 C. Five of the six cages per treatment and cultivar were exposed to the stink bug Euschistus servus (Say). One cage of each treatment contained one of the other species: E. tristigmus (Say), Acrosternum hilare (Say), and Brochymena quadrapustulatus (F.). The most abundant stink bug in West Virginia apple orchards is E. servus (personal observation, MWB) but the other species were included in small numbers to ascertain if there was a complex of species causing damage or just the one species. Two individuals of the same species were added per cage as called for in the experimental design. At harvest, the fruit were picked from inside the cage and brought to the laboratory for evaluation. Stink bug damage was identified by a sunken discolored area on the surface of the fruit, a corky appearance to the flesh below the discolored area, and the presence of a feeding puncture site. Data on percent fruit with stink bug damage were transformed using arcsine (square root) then analyzed with Proc Mixed (SAS Institute 1996) testing for effects of cultivar, treatment, and the cultivar by treatment interaction. The cage design used in 2001 was not sufficient to prohibit feeding completely by stink bugs from outside the cage. Several stink bugs were seen on the outside of the cage feeding through the mesh on fruit inside the cage (personal observation, MWB). To exclude stink bug feeding completely, a revised cage design was used in 2002. Cage diameter was increased to 0.75 m and bamboo stakes were taped to the apple branches to form a support to keep the cage mesh off of the

196 J. Agric. Urban Entomol. Vol. 20, No. 4 (2003) fruit. Thirty Empire trees were selected randomly and, because of a low fruit load, only five Granny Smith trees were selected randomly. Two branches were selected on each tree for caging. One branch had two stink bugs introduced for a two-week period between mid-july and harvest, and the other cage received no stink bugs as a control. A third branch on each tree, with a similar fruit load, also was selected and left uncaged as a control exposed to natural levels of stink bug feeding. Stink bugs were collected and maintained as in 2001. Approximately 80% of the cages with stink bugs contained E. servus, with the rest containing E. tristigmus or E. variolaris (Palisot de Beauvois). At harvest (5 September 2002, for Empire and 30 September 2002 for Granny Smith ) the fruit from the three sample branches were picked and evaluated for damage as in 2001. Because of an inability to normalize the data because of a large number of zeros, the effect of caging on the percent of fruit with stink bug damage was analyzed with the nonparametric median test (Conover 1971). Nutrient content. Beginning at the first cover spray and continuing at about biweekly intervals, calcium chloride was applied with an airblast sprayer to orchards C and I/GC in 2001. A total of 43.7 kg/ha (39 lbs/acre) calcium chloride was applied to Empire trees and 52.7 kg/ha (47 lbs/acre) to Granny Smith in 2001. Twenty randomly selected fruit from each of 15 randomly selected apple trees of each cultivar and from each orchard (a total of 1200 fruit of each cultivar) were picked on 7 September 2001 ( Empire ) and 16 October 2001 ( Granny Smith ) for evaluation in the laboratory. Damage was categorized as caused by stink bug feeding based on morphology of the depression and corky flesh based on descriptions of Mundinger & Chapman (1932) and Rings (1958). If there was doubt about the cause of damage, the damaged area was examined under a dissecting microscope for the presence of a feeding puncture. Percent fruit with stink bug damage was transformed with the arcsine (square root) and analyzed with Proc Mixed (SAS Institute 1996) testing for effects of cultivar, orchard, and the cultivar by orchard interaction. An additional 40 fruit were collected from Granny Smith trees in orchard C on 19 October 2001. Two stink bug-damaged fruit and two undamaged fruit were collected from each of 10 trees randomly distributed in the orchard. No fruit in these orchards exhibited symptoms of cork spot for comparison with stink bug damage. To obtain fruit flesh for nutrient analysis, a hand-operated apple peeler (Back to Basics, Inc., Draper, Utah) was used to first remove the peel and then a sample strip of flesh, 1.5-mm deep 10-mm wide. The fruit flesh was frozen in glass vials covered with parafilm at 80 C until chemical analyses were conducted. Before analysis, the samples were lyophilized for five days, crushed, and transferred to a plastic bag. A 0.5-g subsample was placed in a 15-ml test tube. The subsample was ashed in a muffle furnace for 14 h at 510 to 520 C. After cooling the subsamples to room temperature, 5 ml of 6N HCl was added to digest the subsample and then diluted with 10 ml of deionized water. Subsamples were held in Pyrex tubes covered with parafilm until analysis. Calcium concentration was determined with an atomic absorption mass spectrometer (Leco, St. Josephs, Michigan) under flame (absorption) mode. The equipment was recalibrated against a standard after every 10 samples. An average of three readings was used for analysis. Boron concentration was determined by adding 5 ml concentrated H 2 SO 4 to a 1-ml aliquot from the subsample. The tube was agitated and then 5 ml of carmine solution (0.92 g carmine in 1000 ml of

BROWN: Stink Bug Damage to Apples 197 concentrated H 2 SO 4 ) was added and allowed to react for 45 min. Three 1-ml subsamples were taken and placed into polystyrene cuvettes for analysis with an Ultraspec 3000 UV/Visible Spectrophotometer (Pharmacia Biotech, Piscataway, New Jersey). Readings were taken at 600 nm absorbance and compared with freshly prepared boron standards with an average of the three subsamples used for analysis. Calcium and boron concentrations, no transformation of data was needed, were analyzed with Proc Mixed (SAS Institute 1996) to test for differences between damaged and undamaged fruit. Results and Discussion Characterization of damage. The damage caused by stink bug feeding on apples in the mid- to late season is a depressed, discolored area on the fruit skin. The discoloration appears as a water-soaked to dark green area on both red and green colored cultivars. On red-colored fruit, the discoloration sometimes appears darker red. The area of discoloration is approximately 1 cm in diameter for each feeding site and is roughly circular, but in the case of multiple feeding on the same fruit, the damage may appear larger and irregular. Immediately beneath the depressed, discolored fruit surface is dark, corky flesh that extends about 0.5 to 1 cm into the fruit as shown in Fig. 1A. Although there is a puncture site that provides proof of feeding, this may often be visible only under magnification (Fig. 2). Krupke & Brunner (2001) found that feeding damage to apple by Euschistus conspersus Uhler in Washington was evident within one day of feeding. Stink bug feeding damage differs from cork spot, a calcium related symptom. Corking only occurs immediately adjacent to the fruit skin in stink bug damage (Fig. 1A), whereas in cork spot the damage may occur separate from the skin with healthy flesh between the corking and the skin (Fig. 1B) (Faust & Shear 1968). Corking of the flesh appears more diffuse in cork spot (Fig. 1B), whereas in stink bug damage the corking is uniform within the affected area (Fig. 1A). The fruit surface of cork spot is irregular in outline compared with a more circular appearance in stink bug damage. The depression in cork spot is shallow compared with that in stink bug damage and the edge of the depression is more abrupt in cork spot. Stink bug damage can occur as a single blemish or as multiple sites which often are clustered anywhere on the fruit. Cork spot generally occurs as multiple sites on a fruit, generally more randomly distributed as opposed to clustered, and often is more abundant near the calyx end of the fruit (Faust & Shear 1968). Bitter pit, another calcium deficiency symptom, is different from stink bug damage. Bitter pit most often occurs during storage, whereas stink bug damage does not develop or progress after harvest. Bitter pit appears as small, shallow, irregularly shaped black depressions with only a small extent (2 to 3 mm) of corky flesh under the skin (Faust & Shear 1968). Cage studies. During both years of exclusion cage studies, no stink bug damage was observed on fruit in the orchard prior to caging in early July. Cages made of the same mesh and with similar design were previously shown to have no microclimate effects in the shade, and in full sunlight increased the enclosed branch temperature by only 1 C (Brown 2003). In the 2001 study, treatment effect was significant (F 9.60; d.f. 4, 50; P < 0.0001) but there was no significant effect of cultivar (F 1.77; d.f. 1, 50; P 0.1898) or a cultivar by treatment interaction (F 1.38; d.f. 4, 50; P 0.2549), therefore, data were

198 J. Agric. Urban Entomol. Vol. 20, No. 4 (2003) Fig. 1. Cross section of stink bug feeding damage, A, and cork spot, B, on an unnamed New York cultivar (bars 1 cm).

BROWN: Stink Bug Damage to Apples 199 Fig. 2. Stink bug feeding punctures (P) showing different appearances of the feeding site, lenticels (L) are indicated for reference; A, Granny Smith ; B, Empire (bars 1 cm). pooled for both cultivars. A total of 568 caged fruit were evaluated ranging from 108 to 122 fruit per treatment. The most damage occurred in the two earlier exposure periods: from 48 to 26 days ( Empire ) and 60 to 32 days ( Granny Smith ) before harvest (Table 2). Apparently, fruit between one and two months before harvest either are more susceptible to damage or are more attractive to stink bugs. Damage to fruit exposed to stink bugs for the 15 days ( Empire ) or 17 days ( Granny Smith ) before harvest was nearly twice as high as the control without stink bugs (Table 2), but this was not significantly different due to high variability in damage among cages within each treatment. Similar damage to apples was observed in cages containing all species of stink bugs tested and damage seemed to occur with the same frequency for each species. In 2002, the modified cages were effective at excluding stink bugs and there was no damage on any of the 191 fruit evaluated from the control cages, confirm-

200 J. Agric. Urban Entomol. Vol. 20, No. 4 (2003) Table 2. Effect of timing of exposure to stink bugs on percent fruit damage from 2001 cage experiment, data for Empire and Granny Smith pooled, Kearneysville, West Virginia. Days before harvest exposed to stink bugs (no. fruit) Empire Granny Smith Percent damage ± SEM a 48 36 (103) 60 46 (37) 49.0 ± 5.39a 35 26 (71) 45 32 (38) 53.2 ± 5.74a 25 16 (65) 31 18 (43) 33.5 ± 5.62b 15 0 (68) 17 0 (48) 23.9 ± 5.39bc Stink bugs excluded (73) Stink bugs excluded (40) 11.9 ± 5.62c a Untransformed means presented, analysis done on arcsine (square root) transformed data; mean separation by L.S.D., P 0.05. ing that this damage occurs only in the presence of stink bugs (median test, P < 0.01, d.f. 1). Significantly more damage occurred (median test, P < 0.05, d.f. 1) when stink bugs were enclosed with fruit for a two week period (median 40% fruit damage, range 0 to 100, n 164) as compared with natural infestation levels (median 0% fruit damage, range 0 to 50, n 133). All three species of stink bug tested in 2002 caused similar fruit damage at a similar frequency. Nutrient content. Orchard C, which received CaCl applications, had the greatest amount of stink bug damage, and orchard I, which did not receive CaCl, had the least amount of damage (Table 3). Application of foliar calcium did not reduce this form of damage (F 10.15; d.f. 3,98; P < 0.0001) as it does for cork spot and bitter pit (Shear 1972, Raese & Drake 1993). Fruit flesh just below the skin from damaged and undamaged fruit showed no difference in either calcium (F 0.30; d.f. 1,18; P 0.5910) or boron (F 0.18; d.f. 1,18; P 0.6756) concentration (Table 4), further indicating that this damage is not related to deficiencies in these nutrients. Table 3. Percent stink bug damage to fruit by orchard management, 600 fruit per orchard, (only conventional had a standard insecticide program, the others had a reduced program, see Table 1) and calcium chloride treatment, Kearneysville, West Virginia, 2001. Orchard Calcium Percent damage a Conventional Applied 32.4a Interplanted peach and apple Not applied 16.7c Ground cover flowers under trees Not applied 25.6b Interplanted and with flowers Applied 24.8b a Untransformed means presented, analysis done on arcsine (square root) transformed data; pooled SEM 2.14; mean separation by L.S.D., P 0.05.

BROWN: Stink Bug Damage to Apples 201 Table 4. Calcium and boron concentration in apple fruit flesh just beneath the skin in stink bug damaged and undamaged fruit, Kearneysville, West Virginia, 2001. Calcium (ppm ± SEM) a Boron (ppm ± SEM) a Stink bug damaged fruit 324.8 ± 21.2a 57.9 ± 5.0a Undamaged fruit 341.2 ± 21.2a 63.1 ± 11.0a a Mean separation within columns by L.S.D., P 0.05. The presence of flowering plants in the ground cover of two of the orchards did not have a consistent effect on the amount of stink bug damage to fruit (Table 3). In New Jersey peach orchards, Atanassov et al. (2002) found more stink bugs, and in one year more fruit damage, in orchards with broadleaf weeds than in orchards with better broadleaf weed control. However, I previously found no increase in stink bug damage to peach fruit due to the presence of the same flowering plant species as used in this study (Brown 2002). The ineffectiveness of the insecticide schedule used in this study to reduce stink bug damage, as demonstrated by the highest rate of damage being in the only orchard to receive conventional insecticides, orchard C (Table 3), indicates alternative management tactics may be needed. Stink bugs do cause damage to apples in the mid- to late season. This damage superficially resembles cork spot, a calcium deficiency related problem, but can be distinguished by the external appearance of the damage site, the nature of corking in the fruit flesh, and the presence of a feeding puncture. Proper recognition of stink bug damage to apple fruit in the mid- to late season is becoming more important because of the recent appearance of a potentially serious fruit pest in Pennsylvania, the exotic stink bug Halyomorpha halys (Stäl) (Hoebeke & Carter 2003). As a result of the potential confusion of stink bug damage with the symptoms of calcium deficiency (cork spot), monitoring techniques and methods for stink bug population management are needed to properly manage both stink bug damage and cork spot. Because damage is caused by highly mobile adults and there is a complex of at least five species (E. servus, E. tristigmus, E. variolaris, Acrosternum hilare, and Brochymena quadrapustulatus), management of these pests is likely to be difficult. Acknowledgments The author thanks Clarissa R. Mathews, Stephen S. Miller, and George M. Greene for discussions on stink bugs and cork spot; Dariusz Swietlik for expertise on elemental analysis; and Clarissa R. Mathews, Stephen S. Miller, Ross E. Byers, and Henry W. Hogmire and two anonymous reviewers for comments on an earlier version of this manuscript. References Cited Atanassov, A., P. W. Shearer, G. Hamilton & D. Polk. 2002. Development and implementation of a reduced risk peach arthropod management program in New Jersey. J. Econ. Entomol. 95: 803 812.

202 J. Agric. Urban Entomol. Vol. 20, No. 4 (2003) Borden, A. D., H. F. Madsen & A. H. Retan. 1952. A stink bug, Euschistus conspersus, destructive to deciduous fruits in California. J. Econ. Entomol. 45: 254 257. Bowling, C. C. 1979. The stylet sheath as an indicator of feeding activity of the rice stink bug. J. Econ. Entomol. 72: 259 260. Brown, M. W. 2001a. Is it stink bug or cork spot? pp. 14 15In Proceedings of the 77 th Cumberland-Shenandoah Fruit Workers Conf. Brown, M.W. 2001b. Flowering ground cover plants for pest management in peach and apple orchards. In Proceedings of the International Conference of Integrated Fruit Production. IOBC/wprs Bull. 24: 379 382. Brown, M. W. 2002. Are flowering plants taboo in peach orchards? Proc. Fifth International Peach Symp. Acta Hort. No. 592: 659 662. Brown, M. W. 2003. Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia. USA. Biol. Cont. 29: 189 198. Conover, W. J. 1971. Practical nonparametric statistics. John Wiley & Sons, Inc. New York. pp. 167 172. Faust, M. & C. B. Shear. 1968. Corking disorders of apples: a physiological and biochemical review. Bot. Rev. 34: 441 469. Hoebeke, E. R. & M. E. Carter. 2003. Halyomorpha halys (Stal) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Wash. 105: 225 237. Krupke, C. H. & J. F. Brunner. 2001. Stink bug biology, behaviour and management. Proc 97 th Washington State Hort. Soc. 173 176. Miles, P. W. 1958. The stylet movements of a plant-sucking bug, Oncopeltus fasciatus Dall. (Heteroptera: Lygaeidae). Proc. R. Entomol. Soc. London Ser. A 33: 15 20. Miles, P. W. 1959. The salivary secretions of the plant-sucking bug, Oncopeltus fasciatus Dall. (Heteroptera: Lygaeidae). I. The types of secretions and their role during feeding. J. Insect Physiol. 3: 243 255. Miller, R. H. 1980. The ontogeny and cytogenesis of cork spot in York Imperial apple fruit. J. Amer. Soc. Hort. Sci. 105: 355 364. Mundinger, F. G. & P. J. Chapman. 1932. Stink bugs as pests of pear and other fruits in the Hudson Valley. J. Econ. Entomol. 25: 655 658. Nilakhe, S. S., R. B. Chalfant & S. V. Singh. 1981. Field damage to lima beans by different stages of southern green stink bug. J. Georgia Entomol. Soc. 16: 392 396. Raese, J. T. & S. R. Drake. 1993. Effects of preharvest calcium sprays on apple and pear quality. J. Plant Nutrition 16: 1807 1819. Rings, R. W. 1958. Types and seasonal incidence of plant bug injury to peaches. J. Econ. Entomol. 51: 27 32. SAS Institute. 1996. SAS/STAT User s guide, release 6.03e. SAS Institute, Cary, North Carolina. Shear, C. B. 1972. Incidence of cork spot as related to calcium in the leaves and fruit of York Imperial apples. J. Am. Soc. Hort. Sci. 97: 61 64. Shearer, P. W. & V. P. Jones. 1996. Suitability of macadamia nut as a host plant of Nezara viridula (Hemiptera: Pentatomidae). J. Econ. Entomol. 89: 996 1003. Simons, R. K., F. N. Hewetson & M. C.-Y. Chu. 1971. Sequential development of the York Imperial apple as related to tissue variances leading to corking disorders. J. Am. Soc. Hort. Sci. 96: 247 252. Solymar, B. 1999. Integrated pest management for Ontario apple orchards. Ontario Apple Marketing Commission, Toronto, Canada. 04-99-4M Yates, I. E., W. L. Tedders & D. Sparks. 1991. Diagnostic evidence of damage on pecan shells by stink bugs and coreid bugs. J. Am. Soc. Hort. Sci. 116: 42 46.